Vespa velutina: A new invasive predator of honeybees in Europe

Abstract

The yellow-legged hornet (Vespa velutina) is the first invasive Vespidae predator of honeybees to be accidentally introduced into Europe from Asia. In the current pollinator decline, V. velutina is an additional stressor for honeybees and other pollinators. Although V. velutina contributes to the loss of honeybee colonies, little is known about its biology and behaviour both in the native and in the invaded area. Here, we review the current knowledge of this species and describe its life cycle and life history traits (reproduction, overwintering, foraging and dispersal) in the light of the biology of other Vespidae. We also review the impact of this species on ecosystems, on the economics of beekeeping, and on human health (this species being potentially deadly for allergic people). Based on this information and on previous worldwide experiences with Vespidae invasions, we propose key research topics for the development of effective management plans. We identify methods to limit the impact and proliferation of V. velutina in Europe that are based on nest destruction, trapping, population genetics, and biological control. In our opinion, research effort on the means to detect and destroy V. velutina nests at an early stage is required in order to short-circuit the colony cycle and thus limit both its impact on honeybees and its expansion through Europe. Finally, we discuss the impact of this biological invasion on the development of methods that should be used to manage alien species in the future.

Full text

REVIEW
Vespa velutina: a new invasive predator of honeybees in Europe
Karine Monceau •Olivier Bonnard •
Denis Thie
´ry
Received: 21 May 2013 / Accepted: 6 November 2013 / Published online: 17 November 2013
ÓSpringer-Verlag Berlin Heidelberg 2013
Abstract The yellow-legged hornet (Vespa velutina)is
the first invasive Vespidae predator of honeybees to be
accidentally introduced into Europe from Asia. In the
current pollinator decline, V. velutina is an additional
stressor for honeybees and other pollinators. Although V.
velutina contributes to the loss of honeybee colonies, little
is known about its biology and behaviour both in the native
and in the invaded area. Here, we review the current
knowledge of this species and describe its life cycle and
life history traits (reproduction, overwintering, foraging
and dispersal) in the light of the biology of other Vespidae.
We also review the impact of this species on ecosystems,
on the economics of beekeeping, and on human health (this
species being potentially deadly for allergic people). Based
on this information and on previous worldwide experiences
with Vespidae invasions, we propose key research topics
for the development of effective management plans. We
identify methods to limit the impact and proliferation of V.
velutina in Europe that are based on nest destruction,
trapping, population genetics, and biological control. In our
opinion, research effort on the means to detect and destroy
V. velutina nests at an early stage is required in order to
short-circuit the colony cycle and thus limit both its impact
on honeybees and its expansion through Europe. Finally,
we discuss the impact of this biological invasion on the
development of methods that should be used to manage
alien species in the future.
Keywords Apis mellifera Biodiversity Invasive
species Pest management Vespidae 
Yellow-legged hornet
Introduction
Vespa velutina (Lepeletier 1836), the yellow-legged hornet
(Hymenoptera: Vespidae) is a recently introduced alien
species in Europe. It was observed in southwest France for
the first time in 2004 (Rortais et al. 2010). This is the first
Vespidae predator accidentally introduced from Asia to
Europe (Rortais et al. 2010; Roy et al. 2011) and the
invasive population rapidly raised impressive size, espe-
cially in the west of the introduction area. This biological
invasion has led to several serious problems because V.
velutina preys on the domestic honeybee (Apis mellifera),
disrupts the ecological role of the honeybee, potentially
alters biodiversity, harms commercial beekeeping activities
and is potentially deadly to allergic people. Beyond the
ecological, economic and societal impacts common to all
Vespidae invasions (Beggs et al. 2011), V. velutina inva-
sion in Europe is a novel and dramatic example of the lack
of emphasis on invasive species in Europe and demon-
strates the urgency to establish efficient European policies
to avoid future biological invasions.
Communicated by N. Desneux.
K. Monceau O. Bonnard D. Thie
´ry (&)
UMR 1065 Sante
´et Agroe
´cologie du Vignoble, INRA, ISVV,
33883 Villenave d’Ornon, France
e-mail: thiery@bordeaux.inra.fr
K. Monceau O. Bonnard D. Thie
´ry
UMR 1065 Sante
´et Agroe
´cologie du Vignoble,
Bordeaux Sciences Agro, ISVV, Universite
´de Bordeaux,
33883 Villenave d’Ornon, France
Present Address:
K. Monceau
Equipe Ecologie Evolutive, UMR 6282 Bioge
´osciences,
Universite
´de Bourgogne, 6 Bd Gabriel, 21000 Dijon, France
123
J Pest Sci (2014) 87:1–16
DOI 10.1007/s10340-013-0537-3

Despite this large impact on the whole ecosystem, sev-
eral information about the biology and behaviour of V.
velutina are still lacking. This limited knowledge repre-
sents a considerable disadvantage in the establishment of
management plans. Given the current expanding distribu-
tion of V. velutina, it is increasingly important to identify
research topics that will lead to the development of
effective management strategies. In the present review, we
first present the current situation of V. velutina invasion in
Europe and then we propose a synthesis of the current
literature on the biology and behaviour of V. velutina and
its impact in the new invaded area. The knowledge of V.
velutina is quite limited; hence we also examine the liter-
ature on closely related species in this review. Based on
this information and on other reports of Vespidae invasions
worldwide, we propose several key research areas and
identify management methods that may limit the impact
and dispersal of V. velutina in Europe. Our review is
mostly based on data regarding the invasion of this species
in France, the first European country to be invaded, but our
identification of important research topics may also help
other countries to develop effective methods for manage-
ment of this species.
Origin, invasion and current situation
Most Vespa species are native to Asia, except the European
species, Vespa crabro, and the Oriental hornet, Vespa
orientalis, which is mainly found in the sub-Mediterranean
region (Spradbery 1973; Matsuura and Yamane 1990).
Vespa velutina is common in central to eastern Asia (Ya-
mane 1974; Starr 1992; Abrol 1994; Martin 1995;Car-
penter and Kojima 1997; Nguyen and Carpenter 2002;
Nakamura and Sonthichai 2004; Nguyen et al. 2006) and is
currently spreading throughout Korea (Kim et al. 2006;
Choi et al. 2012).
Vespa velutina was accidentally introduced into south-
west France in a single event, probably via boat transport
from the Zhejiang or Jiangsu provinces of eastern China
(Arca 2012). The first European colony was recorded in
2004 close to Agen, beekeepers soon noted predation on
honeybees in this area and the hornet rapidly colonized
southwest France, followed by an increase in the number of
nests (INPN 2013). Different simulations based on climatic
similarities of locations in France and Asia predicted an
expansion to most parts of France and neighbouring
European countries (Iba
´n
˜ez-Justicia and Loomans 2011;
Villemant et al. 2011a). The comparison between native
and invaded areas shows that they differ in their level of
precipitation during the driest month of the year, the
invaded areas receiving more precipitation than the native
area (Villemant et al. 2011a). Increasing reports have
mentioned V. velutina spread throughout Europe. Nests
have been already destroyed in Spain (Lo
´pez et al. 2011)
where beekeepers have already observed predation on their
colonies in northwest Spain. Individuals have also been
observed in Portugal (Grosso-Silva and Maia 2012) and in
Belgium near the border with France where a flying male
has been observed (Bruneau 2011; Thirion 2012). More
recently, a nest has been destroyed for the first time in Italy
at Vallecrosia near the French border (Demichelis et al.
2013).
Biology and life history traits of V. velutina
Identification and description
Vespa crabro (the European hornet) and V. velutina can be
easily distinguished from each other by their colours:
brown and brownish yellow for V. crabro and black and
yellow for V. velutina (Fig. 1) but also by their size, V.
crabro being the largest (Fig. 1).
Within the species, sex differences in V. velutina are
similar to those observed in other species: the presence/
absence of sting (female/male) and the length of antennae
(Edwards 1980). Indeed, the antennae of females are
shorter and thinner than those of males (Fig. 2). Discrim-
ination between queens and workers is less conspicuous
because there is no apparent colour pattern which differ-
entiates the individuals belonging in these castes. Body
mass cannot be used with high confidence because it is
highly variable across time (see Fig. 5 in Monceau et al.
2013a). Wing shape and size could, however, be used with
more confidence although there is a slight overlap between
queens and workers (Perrard et al. 2012).
Life cycle (Fig. 3)
Like most Vespa species (Spradbery 1973; Matsuura and
Yamane 1990; Takahashi et al. 2002,2004a,b,2007; but
Fig. 1 Queens of Vespa crabro (left) and V. velutina (right)
(ÓK. Monceau)
2 J Pest Sci (2014) 87:1–16
123

see, however, V. affinis, Ross and Carpenter 1991), nests in
the French population of V. velutina are founded by a
single queen (monogynous colonies; Arca 2012). The
queen starts building its nest and rapidly lays eggs. During
this phase (called ‘‘the queen colony phase’’), the queen is
alone and vulnerable until the first workers emerge. Then,
colony and nest size increase throughout the summer. From
spring to autumn, hundreds to thousands of individuals are
produced (in average 6,000 individuals according to
Villemant et al. 2011b). In autumn, the nest reaches its
largest size (see Fig. 4for an example). Autumnal colony
production is mainly focussed on gynes (potential queens)
and males, and most activities are related to mating and
dispersal. On average, three times more males seem to be
produced from mid-September to end November (on
average 350 gynes vs. 900 males; Villemant et al. 2011b).
Although anecdotic observations reported the presence of
living larvae in nests during the winter, only gynes (mated
and unmated) are believed to over-winter (workers and
males die before winter). The next spring, the fertilized
foundresses initiate their new colony, but the fate of the
unmated gynes and their proportion is unknown.
Fig. 2 Individuals belonging
to the different castes in Vespa
velutina (ÓK. Monceau)
Fig. 3 Life cycle of Vespa
velutina in France. The crosses
on males and workers in
December stand for their death
(only gynes survive winter)
(ÓINRA, K. Monceau and D.
Thie
´ry)
J Pest Sci (2014) 87:1–16 3
123

Foraging behaviour
Carbohydrates
Carbohydrates are the main source of energy for adult
vespids (Raveret Richter 2000). These carbohydrates are
provided by flower nectar, tree sap, or ripening fruits,
depending on the environment and season. For example,
in France, V. velutina foundresses often occur on
camellia flowers (Camellia spp.) in spring and males
often occur on ivy (Hedera helix;Fig.5) during autumn.
In southwest France, V. velutina frequently occurs in
vineyards before and/or during grape harvest.
Proteins
Prey spectrum The brood requires animal proteins which
are transformed into flesh pellets and then offered to the
larvae (Raveret Richter 2000). Proteins are collected by the
queen during the queen colony phase and then by the
workers. Vespids are opportunistic generalist foragers and
scavengers, and feed on diverse arthropods, as well as on
carrion, and stalls or waste from butchers and fishmongers
(Spradbery 1973; Edwards 1980; Matsuura and Yamane
1990; Raveret Richter 2000). An analysis of V. velutina
flesh pellets from few nests indicated that Apidae repre-
sented one-third to two-thirds of dietary protein, the pro-
portion of which was suggested to depend on the nest
location and environment (Villemant et al. 2011b). Indeed,
the authors only qualified the nest environment but did not
consider that the hornet hunting sites can differ, hornets
potentially foraging in a large range around their nests (see
‘‘ Foraging range’’ section below).
Hunting behaviour with a special emphasis on honey-
bees Vespa velutina predation on honeybee colonies
increases throughout the summer and continues until the
end of November in parallel with the population size of the
hornet (Monceau et al. 2013a,b); the duration of the colony
cycle might, however, vary according to the extension
towards the north. Apiaries are large food sources that are
concentrated in relatively small areas. Vespa velutina
mainly preys upon flying honeybees that hover in front of
the hive entrance (Abrol 1994; Monceau et al. 2013b). In
Asia, they prey on the native Asian honeybee (Apis cerana)
and on the introduced European honeybee (A. mellifera).
Honeybee anti-predator behaviour against V. velutina has
received a considerable interest because of the contrast
between the native and the introduced species. Indeed, A.
cerana which is likely to have coevolved with V. velutina
exhibits efficient anti-predator behaviours against this
hornet species, whereas A. mellifera suffers higher preda-
tion rate due to the inefficiency of its defence (Ken et al.
2005; Tan et al. 2007,2010,2012a,b,2013). Anti-predator
behaviours in A. cerana include a so-called defensive ‘‘bee-
carpet’’ at the hive entrance, heat-balling and abdomen
shacking movements (shimmering) (Ken et al. 2005; Tan
et al. 2007,2010,2012a,b,2013). With the exception of
shimmering which has never been observed to date (Tan
et al. 2013), A. mellifera is able to exhibit the same anti-
predator behaviours as A. cerana but with lower efficiency.
For example, A. mellifera workers may engulf hornets but
the number of individuals recruited to produce the heat-ball
and the temperature they are able to reach are lower than in
A. cerana colonies (Ken et al. 2005). In Europe, V. velutina
is the introduced species while A. mellifera is the native
one, but the situation is equivalent. Although A. mellifera
Fig. 4 Example of the size of Vespa velutina nest in autumn
(ÓK. Monceau)
Fig. 5 Male Vespa velutina feedingonivy(Hedera helix) (INRA
Bordeaux-Aquitaine research centre, GPS: N44°47018.2000 W0°34046.2600,
September 2011, ÓK. Monceau)
4 J Pest Sci (2014) 87:1–16
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can exhibit the bee-carpet behaviour and engulf hornets,
the sustained and increasing predation of V. velutina from
summer to autumn weakens honeybee colonies and may
lead to increasing colony death rate during winter (Arca
2012; Monceau et al. 2013a,b).
Foraging range
Vespidae are central place foragers which can fly from
50 m to several kilometers from their nests (Edwards 1980;
Matsuura and Yamane 1990). Currently, the foraging range
of V. velutina is still unknown. Knowledge of V. velutina
foraging range is crucial for pest management programme
(Akre and Davis 1978) and could be studied, for example,
by radio-tracking survey. Such data would be of major
interest especially to understand the contribution of sur-
rounding V. velutina colonies to predation on a given
apiary (Monceau et al. 2013a).
Mating behaviour
Monandry is the most common mating system in eusocial Hy-
menopterans (Strassmann 2001), but previous research reported
Vespa queens inseminated by multiple males in at least three
species (V. crabro,V. mandarinia,andV. simillima, Foster et al.
1999; Takahashi et al. 2004a,b,2007). Polyandry occurs from
10 % in V. mandarinia to 40 % in V. simillima (Takahashi et al.
2004a,2007) and most colonies of these species are from a single
queen (monogyny) who mated with a single male. Recent
genetic analysis of nine colonies reveals that in eight of them, V.
velutina gynes mated with several males (Arca 2012). In social
insects, polyandry may be favoured because offspring from
different patrilines have increased genetic diversity (Keller and
Reeve 1994; Boomsma and Ratnieks 1996; Jennions and Petrie
2000). Polyandry could thus be advantageous compared to
monandry in increasing offspring genetic diversity and thus
compensating the low genetic diversity due to the single intro-
duction event (see Arca 2012).
Most gynes and males emerge during the autumn
(Fig. 3). However, recent observations of nests maintained
in laboratory conditions showed earlier production of
males (Monceau et al. 2013c), and this has been confirmed
by the presence of males captured in traps around hives
during the early summer (Monceau et al. 2013a). Addi-
tionally, in captivity agonistic behaviours of workers
against males were observed (Monceau et al. 2013c),
which could be related to mating with kin avoidance (Ta-
badkani et al. 2012). This behaviour has, however, to be
confirmed in the wild. Such agonistic behaviour has
already been reported in V. simillima (Matsuura and Ya-
mane 1990) and also occurs in the invasive paper wasp
(Polistes dominulus). In this species, females accept to
mate more often with non-nestmate than with nestmate
males which in consequence limit inbreeding (Liebert et al.
2010).
Depending on the Vespa species, mating may occur
around the nests (and probably inside nests) and/or else-
where (Matsuura and Yamane 1990; Ross and Carpenter
1991). For example, V. mandarinia males stay near the nest
entrance and wait for emerging gynes, but males of other
species may wait for females in other areas (Matsuura and
Yamane 1990). So far, only few anecdotal observations of
V. velutina copulations outside the nest have been reported
(in captivity, N. Maher, pers. com.; on a sunny pavement,
K. Monceau, pers. obs.). Additionally, male behaviour
during autumn may argue for mating occurring outside the
nest. Indeed, V. velutina males often occur on flowering
plants, especially ivy (H. helix; Fig. 5), but the function of
this attraction is unknown. Although they may forage for
their own sustenance during their search for mates (ivy
being a well-known autumnal source of nectar and pollen
for many insects, Spradbery 1973), the plants visited by
males during the autumn may represent a resource-based
rendezvous site that improves their mating frequency
(Ayasse et al. 2001; Boomsma et al. 2005; Spiewok et al.
2006). If so, then gynes should also occur on these plants.
This hypothesis deserves further investigation because, like
other social wasps, V. velutina may adopt resource defence
polygamy (i.e. males patrolling in the female foraging
range), with the gynes emerging asynchronously (Boom-
sma et al. 2005). Although resource defence polygamy may
suggest the presence of competitive interactions between
vespid males, this kind of interaction seems to be rare
(Ross and Carpenter 1991) and no record of such behaviour
has been reported so far for V. velutina.
Regardless of the mating location, sexual pheromones may
play a role in mating. In social vespids, they can be produced
by the males and the females (reviewed in Downing 1991;
Ayasse et al. 2001). Although there is evidence for sex
pheromone biological activity in several Vespa species (Ono
and Sasaki 1987; Spiewok et al. 2006) and to a further extent
in Vespidae, no specific sexual pheromone has yet been
identified (Ayasse et al. 2001; Spiewok et al. 2006). Thus,
focussing on sexual pheromones in V. velutina is an important
task and would present interesting application to limit mating
and thus to control populations. Several glands have been
identified as potential source of sex pheromones such as
venom gland in females (Post and Jeanne 1983; Keeping et al.
1986) and mandibular and/or sternal glands in males (Reed
and Landolt 1990). Testing the secretion produced by these
glands in V. velutina could therefore represent a first step to
consider.
J Pest Sci (2014) 87:1–16 5
123

Foundress dispersal, overwintering and emergence
from overwintering
At the end of autumn, gynes search for hibernation sites
outside the nest. They could be either mated or not; the
proportion of mated ones is still unknown. Depending on the
species, vespid foundresses hibernate in the soil or tree cre-
vices (Edwards 1980; Matsuura and Yamane 1990; Vetter
and Visscher 1997)andV. velutina foundresses have been
observed in woodpiles, shelters, or burrows during the winter.
The dispersal range of V. velutina queens is not known, but
the annual expansion range appears large and most probably
favoured by passive dispersion through human-mediated
transport (for example, in trucks transporting goods). How-
ever, it is not possible to separate natural from passive dis-
persion in the spatial expansion of this species. Evaluating
and/or monitoring human-mediated dispersal would be diffi-
cult at least for two reasons: first such a dispersal occurs most
of the time accidentally and second it represents a consider-
able amount of traffic through the French territory since
France is a crossroads between eastern and western Europe.
Surprisingly, despite the fact that nest locations were
recorded since 2004 in a French national database (INPN
2013), no predictive mathematical model of spatial
expansion has been yet produced. Such an approach is, to
our opinion, dramatically missing even though different
studies attempted to evaluate the expansion risk as a
function of climatic similarities with the native area of the
hornet and climate change scenario (Iba
´n
˜ez-Justicia and
Loomans 2011; Villemant et al. 2011a; Barbet-Massin
et al. 2013).
Like in other insects, abiotic conditions (temperature,
day-length), genetic background, and endocrine levels
affect the overwintering process in Vespidae (Spradbery
1973; Edwards 1980; Matsuura and Yamane 1990), but this
has received too little attention. In Polistes dominula, the
termination of diapause seems unrelated to the level of a
juvenile hormone (JH) per se, but instead individual
foundresses seem to have varying sensitivity to JH (Tibb-
etts et al. 2011). The overwintering of V. velutina ends in
early spring, and foundresses fly from mid-March to late-
June (Monceau et al. 2012,2013a). Other research has
documented long queen colony phase (see ‘‘Life cycle’’
section) in V. crabro, for example (Spradbery 1973).
Variability in the duration of overwintering in other insects
is documented as a ‘‘bet-hedging’’ strategy that may allow
for adaptation to new or uncertain environments (Gour-
bie
`re and Menu 2009) which is required for alien species
colonizing new environments.
Nesting behaviour
Nest location
The characteristics of Vespidae nests vary among the dif-
ferent species (Edwards 1980; Matsuura and Yamane
1990). According to Kemper (1960), temperature, humid-
ity, light intensity, shelter from rain, and shelter from wind
are important for nest site selection because these factors
determine the nest preservation which is essential for col-
ony survival. Vespidae build papier-ma
ˆche
´nests by mixing
plant fibres with water and saliva and add new layers over
time (Edwards 1980), so easy access to suitable wood
fibres is crucial. Vespidae may collect rotten or dead
material from trees (Edwards 1980; Matsuura and Yamane
1990; Martin 1995), but no specific plant resource has been
yet identified for V. velutina nest building, and it may
depend upon the hornet species and the environment. In
France, nests are often seen in poplars, which grow in
riparian forest, i.e. in close vicinity to river. These trees
may provide both a support and be located in close vicinity
to a source of water for nest building. Indeed, queen
trapping experiments in spring confirm that V. velutina
foundresses occur mainly nearby water (Monceau et al.
2012). Initially, an analysis of the characteristics of the nest
sites should help to identify the most important factors
among those we have cited and thus defining the most
suitable place for nest installation.
Vespa velutina nests are established either in or on tree
tops, bushes, shrubs, roofs, and eaves in urban areas, and
may also be underground (Edwards 1980; Starr and Jac-
obson 1990; Starr 1992; Martin 1995; Nakamura and
Sonthichai 2004; Abrol 2006; Kim et al. 2006; Choi et al.
2012). Differences in the height of nests may be explained
by the relocation of the colony (i.e. translocation of the
entire colony from the embryo nest to a more suitable
location for colony expansion; Matsuura and Yamane
1990). This behaviour occurring in Taiwan and South
Korea (Matsuura 1991; Choi et al. 2012) is also expected to
occur in Europe, but has not been yet documented to our
knowledge. High nest locations mean that the workers must
expend large amounts of energy for costly upward flight
with a load (prey, nest material, or water). Thus, the
increased cost should be balanced by other fitness gains
like nest protection against enemies. Indeed, lower nests
are more likely to be destroyed by humans because of their
accessibility and thus, human destruction may lead to more
nesting in treetops, with obvious consequences for V.
velutina management.
6 J Pest Sci (2014) 87:1–16
123

Does competition between queens occur?
Intra- and inter-specific competition between foundresses
(including competition for nesting sites and nest usurpa-
tion) could be considered a key factor that regulates pop-
ulation dynamics in Vespa species (Spradbery 1973;
Edwards 1980; Matsuura and Yamane 1990;Ro
¨seler
1991). Such agonistic interactions are often evocated to
discredit the reduction of queens by capture plans in spring
(Haxaire and Villemant 2010), but to our knowledge no
published data clearly shows such competition in France
between V. velutina queens or between V. velutina and V.
crabro queens. In spring 2013, two V. velutina nests have
been observed in a garden shed, spaced half a meter from
each other and surrounded by two P. dominula nests
(Fig. 6). Although this observation is still anecdotic, it may
question the hypothesis of intra-specific competition reg-
ulating alien hornet population. Inter-specific competition
is also less likely to occur since it seems to be rare in areas
where several Vespa species occur (Matsuura and Yamane
1990). Competition between V. velutina and V. crabro or
wasp species (Fig. 6) has never been reported although this
point should be clarified to estimate the potential threat of
the alien on the native species.
Consequences of V. velutina invasion
Social Hymenopterans tend to be successful in invading
new environments because their social organization allows
a high degree of flexibility (Moller 1996; Wilson et al.
2009). In fact, many Vespidae have been reported as alien
species worldwide (Cervo et al. 2000; Matthews et al.
2000; Beggs et al. 2011). The introduction of these species
has had significant impact on the local ecology, economics,
and human health (Beggs et al. 2011). Despite this, the
impact of V. velutina in France has not been well-
documented.
Impact on ecosystems
Predation
Although the causes and extent of the current pollinator
decline is still debated (Ghazoul 2005a,b; Steffen-Dew-
enter et al. 2005; Biesmeijer et al. 2006), a decline of bee
populations occurs in the northern Hemisphere (Brown
2011; Cameron et al. 2011; Bommarco et al. 2012). The
introduction of alien parasite or predator species is one
possible cause of this decline (Brown and Paxton 2009;
Stout and Morales 2009; Schweiger et al. 2010). As pre-
viously evoked (see ‘‘Prey spectrum’’ section), bees have
been observed to represent at least a third of the diet of V.
velutina, but we do not yet have an accurate assessment of
the consequence of the predation by V. velutina on polli-
nation services. Considering the ecological and economic
importance of pollinators, V. velutina is a particular con-
cern. Surveys are therefore needed to locally assess the
impact of V. velutina on pollination services either in dif-
ferent environmental conditions but also in interaction with
other factors (i.e. parasites of bees, floral diversity,
pesticides).
Intra-guild relations
Usually, the introduction of an alien predator can lead to
displacement (i.e. niche exclusion) or replacement of the
native predator from the same ecological guild (Snyder and
Evans 2006). This may be caused by competition for the
same resources, aggression between species, lower vul-
nerability of the alien species to native predators, or greater
vulnerability of the native species to pathogens that were
introduced with the alien (Snyder and Evans 2006; Kenis
et al. 2009; Stout and Morales 2009; Crowder and Snyder
2010).
In the invaded areas of France, V. velutina may interfere
with the European hornet (V. crabro), which is protected in
some areas of its native range (e.g. in Germany since 1987,
Federal Species Protection Ordinance—BArtSchV/Federal
Nature Conservation Act—BNatSchG). Vespa crabro
preys on diverse arthropods and is considered a beneficial
organism in agriculture (Spradbery 1973; Matsuura and
Yamane 1990). However, V. crabro can also prey upon
honeybees (Baracchi et al. 2010), and be a direct compet-
itor of V. velutina in apiaries where these species coexist.
Moreover, since the introduction of V. velutina, some
beekeepers have reported increased V. crabro predation on
honeybees in southwest France. This feeds the hypothesis
that V. crabro may benefit from the presence of V. velutina
by facilitating prey access in weakening honeybee colony
defences. We suggest that future studies investigate the
Fig. 6 Two nests of Vespa velutina (2,3) in close vicinity each other
and cohabiting with two other nests of Polistes dominula (1,4). Vespa
velutina nests are at 55 cm distance each other and the two nests of P.
dominula are at about 15 cm distant to the hornet nests. (The picture
was taken in May 2013 in a garden shed in Navailles-Angos, GPS:
N43°23043.5300 W0°19056.9100,ÓK. Monceau with the courtesy of
Mr Jacques Tardits)
J Pest Sci (2014) 87:1–16 7
123

interaction between these two species and an eventual shift
of habits in V. crabro as a consequence of V. velutina
invasion.
Alternative prey and/or host for native species
Several organisms are known to feed upon and/or exploit
Vespidae (Spradbery 1973; Edwards 1980; Matsuura and
Yamane 1990). Some mammal and bird predators that
inhabit the invaded areas prey upon Hymenopterans
(including V. crabro), such as the Eurasian jay (Garrulus
glandarius), the European bee-eater (Merops apiaster), and
the European badger (Meles meles) (Spradbery 1973;
Edwards 1980). A unique observation of the predation of
V. velutina nest has been realized very recently in south
west France near Bordeaux. The nest has been attacked and
destroyed by a honey buzzard (Pernis apivorus), which is
known to prey on hymenoptera nests (Vigneaud 2013).
Additionally, domestic chickens (Gallus gallus domesticus)
have been observed predating on V. velutina chasing in
apiaries in south west France (Lescoutte-Garden 2013). A
recent study identified V. velutina as potential additional
host in China for the Israeli Acute Paralysis Virus (IAPV)
which infects A. mellifera in China but also in France
(Blanchard et al. 2008; Yan
˜ez et al. 2012). However, to
date, there is currently no more evidence for predation or
parasitism in France.
Effects on apiculture and economics
Impact on honeybee colonies
Vespa velutina predation on honeybees has clearly a direct
economic impact on apiculture but, probably because the
invasion is recent, sociological and economic studies
quantifying this impact are lacking. In one report, a bee-
keeper claimed to have lost up to 80 % of his hives due to
V. velutina predation (Cazenave 2013). Only a few recent
estimates by beekeeper unions are available. In Gironde
(southwest France), 30 % of hives were weakened and/or
destroyed by V. velutina in 2010 (http://www.unaf-
apiculture.info). One of the local beekeeper unions repor-
ted 7.5 % fewer hives during 2011 (7,110 in 2010, 6,576 in
2011) and almost 26 % fewer beekeepers insuring their
hives (218 in 2010, 161 in 2011; Saunier 2011). In
Dordogne, an epidemiological study (questionnaires sent to
beekeepers) of 1,979 hives in 2009 and of 1,991 hives in
2010 indicated that ca. 5 % of the hives were destroyed by
V. velutina each year, and that 16 and 27 % of the hives
were weakened in 2009 and 2010, respectively (B.
Darchen, pers. com.). These data should, however, be
interpreted carefully, because not all beekeepers are pro-
fessionals and not all of the hives were registered, making
the economic impact difficult to quantify. Clearly, the real
impact appears much more over these data although no
scientific publication is available. Moreover, it is difficult
to distinguish damage from V. velutina from other factors
that threaten A. mellifera colonies, such as parasites,
viruses, habitat loss or fragmentation, insecticides and
pesticides, and climate change (Cox-Foster et al. 2007;
Brown and Paxton 2009; Johnson et al. 2010; Le Conte
et al. 2010; Potts et al. 2010; vanEngelsdorp and Meixner
2010; Henry et al. 2012).
Other societal impacts
Another societal impact to consider is the cost associated
with destruction of V. velutina nests. This task, mainly
carried out by beekeepers, is risky, time-consuming, and
expensive. In 2011, one French beekeeper union (GDSA)
coordinated the destruction of more than 1,000 V. velutina
nests in Aquitaine. Destruction of each nest took an aver-
age of one hour (displacement not included). In the geo-
graphical area of Toulouse (southwest France), a company
specialized in pest eradication destroyed ca. 500 V. velutina
nests in 2011. Such action cost €110 per nest and requires
two visits: first to kill V. velutina by spraying insecticide
powder directly into the nest, and second for removing the
nest 1 week later to ensure that all individuals have
returned to the nest and to avoid potential animal poisoning
(E. Savary, pers. com.). There are reports that private
companies have very high costs for nest destruction (over
€500). Currently, these costs are mainly supported by the
citizens, although some municipalities financially
contribute.
Human health
Vespa velutina also has a direct impact on humans because
colonies can occur in populated regions, and the occa-
sionally spectacular size of the nests can generate frenzy.
However, in contrast to its native range of Asia, where it is
considered particularly aggressive with little provocation
(Martin 1995), V. velutina in non-native regions is not
considered to be aggressive when chasing or foraging.
Since 2004, three deaths have been attributed to V. velutina
stings. A recent study by the French Poison Control Centre
reported only one confirmed human death due to V. velu-
tina stings from 2007 to 2010, and no significant increase
in Hymenoptera stings after its introduction (de Haro et al.
2010). However, the actual impact may be greater because
many Hymenoptera stings are not reported. Moreover, the
French media may contribute to the frenzy surrounding
rare events. Finally, the number of deaths due to the ana-
phylactic shock from other Hymenoptera stings is not
reported, so comparison with V. velutina is impossible.
8 J Pest Sci (2014) 87:1–16
123

Pest management
Since the nineteenth century, several management plans
have been tested worldwide against invasive vespids, but
most attempts at eradication have failed (Beggs et al.
2011). In fact, eradication is generally considered impos-
sible when an invasive vespid has widespread distribution.
Assuming that total eradication is no longer possible and
that geographical dispersal is still in progress, V. velutina
management plans could target different stages of the life
cycle (Fig. 3) and could involve: (1) nest destruction; (2)
trapping of workers and queens; (3) control of reproduc-
tion; and (4) biological control.
In this section, we review the current pest management
of V. velutina to identify promising techniques that should
be undertaken or reinforced. We also identify several
methods that should be investigated based on past experi-
ences with vespid invasion worldwide.
Nest destruction
Nest destruction (mechanically or chemically in using
insecticides or biocide gas like sulphur dioxide injected in
the nest) can be an effective method to control pest pop-
ulations (Thomas 1960; Spradbery 1973), but would only
be effective if all individuals, especially the queens, are
destroyed so that the colony does not simply relocate.
Ideally, all detected nests must be destroyed and removed
as soon as possible to limit the impact on apiaries and the
production of reproducers. However, in practice, complete
destruction is almost impossible because most of the nests
are cryptic until they reach a large size. Another problem is
that newly emerged gynes may leave the nest while it is
being destroyed. In such cases, the efficacy of nest
destruction is very limited.
The number of nests actually reported to the French V.
velutina nest database (INPN 2013) depends on the quality
of the observation network. Scientists in charge of this
database report that at least one-third of the public identi-
fications are wrong (Rome et al. 2011). The inaccuracy of
this database is suspected to increase as a function of the
pest extension. Indeed, during the past 2 years, thousands
of nests have been destroyed in southwest France, partic-
ularly those near human activities (schools, houses, etc.).
However, nest destruction is neither locally nor nationally
coordinated, making complete and relevant information
about the number of destroyed nests unavailable.
Trapping individuals
Hornets can be trapped using food baits (carbohydrates or
proteins). Those traps can be used for monitoring (see for
example, Monceau et al. 2012,2013a) or for destruction
(mass trapping or traps baited with insecticides). Insecti-
cides are currently assayed both for their direct and indirect
effect (the adult hornet bring small doses of insecticide
back to the nest) (Thomas 1960; Spradbery 1973; Edwards
1980; Beggs et al. 2011). To date, only traps baited with
food are used to catch V. velutina (workers and queens),
because this is a simple and inexpensive method that
everybody can use. Insecticide-based baits have been used
to control alien wasp species, and have effectively reduced
invasive Vespula populations by up to 99.7 % (see Beggs
et al. 2011 and references therein). Nevertheless, this
method requires that the toxic bait only targets the alien
species or is coupled with a specific attractant to avoid any
side effect on other species. Presently, no such product is
available for V. velutina.
Trapping V. velutina workers to protect apiaries
The protection of beehives is currently the major concern.
This can be achieved by placing lure traps in their vicinity.
Obviously, apiary protection must allow trapping and/or
killing of hornets but not honeybees. To date, beekeepers
have used direct mechanical destruction (killing of hornets
flying in front of their hives) and traps baited with carbo-
hydrates (apple juice, for example Monceau et al. 2013a)or
proteins. Nevertheless, such trapping should be considered
as a local preventative rather than a real solution for lim-
iting the dispersal of V. velutina. Depriving hornets and
their brood from their major food source may also limit
population size. However, V. velutina does not feed
exclusively on honeybees and any possible risk of prey
shift (e.g. to wild bees) should be considered. Nevertheless,
we should note that food traps are not selective and should
be used cautiously to limit the impact on non-target species
(Monceau et al. 2013a).
Trapping V. velutina queens
Queens are responsible for the establishment of new col-
onies, so they are optimal targets for V. velutina manage-
ment. Queen trapping can be performed before and/or after
hibernation (Fig. 3).
During autumn and the beginning of winter, the gyne
population is at its largest, so this is a good time for
trapping. This kind of trapping has been used in New
Zealand, which was invaded by the European wasp
(Vespula germanica) in the 1940s (Thomas 1960). In 1948,
the New Zealand Department of Agriculture paid a bounty
for each queen, and this led to the collection of 118,000
individuals. Unfortunately, this had no significant effect on
the population density in the following year (Thomas
1960). Thomas (1960) postulated that this occurred simply
because a single queen is sufficient for nest establishment.
J Pest Sci (2014) 87:1–16 9
123

For example, the survival rate of Vespula vulgaris queens
has been estimated only 0.01 % (Archer 1980), making
natural selection probably more efficient than human
trapping.
According to Spradbery (1973), the most critical stage
of the V. velutina life cycle is nest initiation by a single
foundress during spring. Spring trapping of queens has
been used in southwest France since 2007 and beekeepers
unions currently promote this technique (Blot 2009). This
method employs sweet bait that is mixed with beer (alcohol
is supposed to repel honeybees) to lure foundresses. Nev-
ertheless, spring queen trapping is controversial because of
possible collateral damage to the entomofauna (Monceau
et al. 2012). As far as agricultural activities are concerned,
the use of pest trapping always has a potential effect on
biodiversity, as the entomofauna (mostly dipterans)
undoubtedly suffers from spring queen trapping (Dauphin
and Thomas 2009; Haxaire and Villemant 2010; Monceau
et al. 2012), and possibly from trapping at other times of
year. This method is also questionable because its efficacy
appears limited (Haxaire and Villemant 2010; Monceau
et al. 2012). Currently, this controversy has not been
resolved. Indeed, like for trapping before hibernation,
reliable data about the efficacy of queen trapping are
missing.
Limiting the reproduction: exploiting the Allee effect
Exploitation of the Allee effect (decrease in per capita
population growth due to reduced population density;
Courchamp et al. 1999) has been proposed as a manage-
ment tool for alien species (Liebhold and Tobin 2008;
Tobin et al. 2011; Suckling et al. 2012). The Allee effect
may be mediated by reduced mate availability and/or
inbreeding depression (Liebhold and Tobin 2008). This
could be achieved in V. velutina by: (1) trapping queens
(see above); (2) trapping males, and/or (3) mating
disruption.
Trapping males using pheromones could reduce the
number of potential mates and increase the proportion of
unfertilized queens. In Hymenopterans, fertilized eggs
develop into diploid females and unfertilized eggs develop
into haploid males (haplodiploidy). Thus, unfertilized
queens would still produce males, so the effectiveness of
such method is doubtful (Fauvergue et al. 2007; but see
Fauvergue and Hopper 2009). Nevertheless, this method
could increase inbreeding and lead to the production of
sterile diploid males. As previously stated, V. velutina
invasion occurs as a single event, so the population has low
genetic diversity due to the founder effect (Arca et al.
2011; Arca 2012). Although males are mostly haploid,
some of them can be diploid due to complementary sex
determination, particularly in inbred populations (see
Fig. 1 in Liebert et al. 2010 for an explanation). Diploid
males are often sterile and impose a large fitness cost on the
colony (Liebert et al. 2004), potentially leading to an
extinction vortex (Zayed and Packer 2005). Diploid males
have been already reported in French populations of V.
velutina (Arca 2012). However, male trapping can be
considered solely if the attraction of mate depends on the
production of female pheromones.
Another possibility for exploitation of the Allee effect is
mating disruption (i.e. altering the communication between
males and females during reproduction to prevent them
from finding mate; Carde
´and Minks 1995; Witzgall et al.
2010) by use of sex pheromones. However, no sex phero-
mones have yet been identified in V. velutina and we do not
know exactly where mating occurs. In general, mating
behaviour and male behaviour are poorly characterized in
this species, so research on these topics should be very
useful.
Biological control
As previously stated (see ‘‘Alternative prey and/or host for
native species’’), several natural enemies are potential
candidates for biological control of V. velutina. At present,
there are few known potential predators of V. velutina,but
parasites can also be used as biological control agents. An
alien species can be free of parasites, parasitized by its
native species, or may acquire parasites from its new
environment. Parasites can have important roles in the
success of an alien invasion and in population growth
(Prenter et al. 2004; Dunn 2009). Indeed, since V. velutina
and A. mellifera had not enough time to coevolve in
France, V. velutina did not adapt to the endemic parasites.
It is possible that V. velutina could be affected by the native
parasites from V. crabro, native honeybees, and/or other
pollinators. For example, honeybees are infected by several
microparasites (microsporidia, viruses, fungi and bacteria)
and macroparasites (parasitic mites; Schmid-Hempel
1995), so these species may also infect V. velutina. For
example, V. velutina may be vulnerable to IAPV, which is
present in France (Blanchard et al. 2008). In Asia, the
Trigonalid parasitic wasp Bareogonalos jezoensis is a
parasite of V. velutina (Matsuura and Yamane 1990).
However, the presence of this parasitic wasp species has
never been reported in France and its involvement in bio-
logical control for V. velutina cannot be considered since it
also parasitizes V. crabro. Alternatively, the release of new
parasites or viruses of V. velutina in France may have
profound effects on other species. Thus, identification of
10 J Pest Sci (2014) 87:1–16
123

the organisms able to parasitize V. velutina may allow
selecting potential biological control agents, but these
biological control agents may be transmissible to native
species.
Overall, the main limitation for developing a biological
control programme for V. velutina is our poor knowledge
of its basic ecology and biology. Consequently, biological
control cannot be considered until such basic investigations
are conducted.
Selection for resistant honeybee colonies
Surprisingly, the parallel between V. velutina and the par-
asitic mite Varroa destructor has never been realized.
Indeed, varroa mites parasitize A. cerana in Asia and have
been transmitted to A. mellifera colonies imported to Asia.
This mite then spread worldwide with its new host, and
invaded European countries in late 1960s (de Guzman et al.
1997; Oldroyd 1999; Sammataro et al. 2000; Rosenkranz
et al. 2010; vanEngelsdorp and Meixner 2010). This mite
feeds on the bee hemolymph and causes significant harm at
the individual and colony level (Genersch 2010; Rosenk-
ranz et al. 2010; vanEngelsdorp and Meixner 2010). Like
A. cerana displays efficient anti-predator behaviour against
V. velutina, this honeybee species displays hygienic and
grooming behaviours that decrease the number of varroa
mites (Boecking and Spivak 1999; Rath 1999; Rosenkranz
et al. 2010). Although feral honeybees have been managed
to obtain Varroa-resistant colonies (Bu
¨chler et al. 2010;
Rosenkranz et al. 2010), unmanaged European honeybees
have also developed resistance in recent years, based on
reports in France (Le Conte et al. 2007) and Gotland
Sweden (Fries et al. 2006). This suggests that natural
selection has favoured the development of a honeybee
defence or resistance mechanism (Fries and Bommarco
2007). Artificial selection may also play a role in mite
resistance, but the heritability of traits such as grooming
and other hygienic behaviours appears to be low, so this
topic requires more investigation (Bu
¨chler et al. 2010;
Rosenkranz et al. 2010).
Just as the invasion of V. destructor almost four decades
ago had a significant impact on beekeeper activities, the
invasion of V. velutina represents an additional source of
stress for honeybee colonies in the current pollination
decline. In France for instance, beekeeping has a long
history of selection for colony docility, but selection for
more defensive honeybees may be a strategy to limit V.
velutina predation. Research on the behavioural charac-
teristics of resistant colonies should be very fruitful.
Indeed, honeybee colonies can differ significantly in their
collective behaviour (Wray et al. 2011), and some colony
behaviours may more effectively limit V. velutina preda-
tion. Thus, selection for colony defensiveness and other
behavioural traits should be considered as a strategy to
reduce the impact of V. velutina.
Pest management policies
The invasion of V. velutina in Europe presents a practical
challenge to current policies regarding management of
invasive species. Indeed, our experience with V. velutina
highlights the importance of early reaction following a pest
introduction, a key parameter that affects the success of
pest management (Myers et al. 1998). The success of the V.
velutina invasion indicates that France, like several other
European countries, does not have an effective preventive
programme in place. This is in contrast to some other
countries, which have strong pest preventive programmes
(e.g. surveillance and quarantine programmes). In partic-
ular, island countries often have strong preventive pro-
grammes because they are aware that insular biota are more
vulnerable to biological invasions (Reaser et al. 2007;
Yoshida 2008). Australia is now the only country world-
wide to be free of varroa mites and this is probably the
result of their acute surveillance programmes (Clifford
et al. 2011).
According to Myers et al. (2000), eradication can often
be considered at the early stage of an alien invasion. In
winter 2012, the French government legally classified V.
velutina as a noxious pest species. As of December 26,
2012 (Journal Officiel de la Re
´publique Franc¸aise 2012), V.
velutina is registered as ‘‘class 2 health hazard’’ (i.e. pre-
vention, surveillance and/or management are not obliga-
tory, but may be realized in the collective interest). To date,
some neighbouring countries (Switzerland and the UK for
example) have already proposed assessment risk plans or
developed response programmes to manage the eventual
invasion of this species (Pe
´re
´and Kenis 2010; Marris et al.
2011) even though the pest did not yet enter these
countries.
At the European level, invasive species policies are
diverse, with little coordination within and between
member states, and this may favour the proliferation of
alien pests (Commission of the European Communities
2008; Shine et al. 2010; Keller et al. 2011). One of the most
promising methods would be the enhancement of European
border controls to limit invasions into new countries
(Bacon et al. 2012). On April 20, 2012, the European
Parliament adopted resolution EU 2020 Biodiversity
Strategy [2011/2307(INI)], which included a directive
concerning invasive species policy. A legislative proposal
establishing European common policy has been released on
September 9th, 2013 and should be soon examined by the
European Council and Parliament before being adopted
(European Commission 2013).
J Pest Sci (2014) 87:1–16 11
123

Concluding remarks
Several lessons can be drawn from V. velutina invasion.
First, European policies should be improved to avoid a
novel dramatic invasion. The experience of Australia with
V. destructor (Australia is still the only country free of
varroa, thanks to the effectiveness of its policies) is prob-
ably the best example to illustrate that point. Second, the
knowledge of the biology and behaviour of the alien
species is essential to establish management plans. In the
current context, our lack of efficacy is mainly due to our
lack of knowledge of the animal. Filling this gap of
knowledge will considerably enhance our chance to man-
age the invasive population of V. velutina properly and thus
to protect honeybees. Human, technical and obviously
financial resources are especially needed and should be
rapidly accessible. Third, whatever method is ultimately
deemed effective, a well-organized and widespread control
Table 1 Summary of
important key research topics
for the management of Vespa
velutina invasive populations
a
Items on which researches
have already started
b
SO
2
is not considered a
biocide by the European Union
directive 98/8/CE and it is not
legally used to kill hornets. In
France, it has been authorized
for a 120-day period in 2013
(Journal Officiel de la
Re
´publique Franc¸ aise 2013)
Nest detection and destruction
Nest detection Studies on colony behaviour/dynamics
a
Determination of nest site characteristics
Destruction methods Find suitable and authorized biocides
b
Foraging range
Foraging range around the
nest (central place foragers)
Mean foraging range
Amount of prey (number of apiaries within the range)
Resource-based rendezvous sites for reproduction
Queen dispersal/pattern of expansion
Colonization history Identify the colonization pathway(s)
Identify the mean of dispersal (natural/human-mediated/both)
Monitoring the invasion
(space and time)
Predictive spatial model of local/national expansion
a
Determine the risk of invasion in neighbouring countries
a
Management network Identify the most suitable actors to lead the management plan
Coordination of the beekeepers
Coordination between member states of the European Union
International database for nest localization (open access for
all actors)
Chemical communication
Sexual pheromones Knowledge of the sexual behaviour of V. velutina
a
Sexual pheromone characterization
Male trapping
Mating disruption
Pheromones Trap selectivity/attractiveness/repellency
a
Kairomones Food preferences
a
Trap attractiveness
a
Honeybee behaviour
Strategies to defend/cope
with predation pressure
Profile of resistant colonies
a
Heritability of the behaviours
Selection based on defensiveness
Pathogens and predators
Natural enemies Find native predator/parasite candidates
Biological control Susceptibility to honeybees and/or V. crabro pathogens
Disease transmission from
hornet to native species
Sanitary status survey of V. velutina populations
Ecological costs of the predation
Trophic chain Impact on honeybee colonies (stress of the colony/the queen)
a
Impact on pollination services
Intra-guild relations With V. crabro (competition, facilitation?)
a
Competition with other insect predators
Native predator/parasite Impact on population dynamics of native predator and parasites
12 J Pest Sci (2014) 87:1–16
123

plan must be implemented as soon as possible for the
whole invaded area, because re-invasion will always occur
from adjacent untreated regions, so widespread and well-
coordinated plans are needed.
Obviously, funding dedicated to V. velutina research is
not unlimited and priorities should be considered (see
Table 1for a summary). At the present time, to our
knowledge, several research teams in France and Spain are
already engaged on trap design and on the identification of
attractants and/or pheromones. One promising lead which
should also be promoted is the early and systematic
detection and destruction of nests to short-circuit the col-
ony cycle. However, even if the number of nests increases
and the detection tools progress, finding them early in the
season is like looking for a needle in a haystack and would
require a large human and financial investment.
Finally, V. velutina is the first invasive species to have
received significant media attention in Europe, probably
because its preferred prey, the honeybee, is a symbol of
biodiversity and because many people are afraid of wasps
and hornets. However, we currently lack accurate and
reliable data on the effects of this new alien species on
ecosystems and human activities. Initial simulations sug-
gest that this species will soon disperse throughout Europe
and along the Mediterranean coast, so it will likely have a
drastic impact in countries in which there is significant
apiculture, if not managed before.
Acknowledgments This review was invited by Dr. Nicolas Des-
neux, subject editor of the Journal. Our research project on V. velutina
is currently funded by Re
´gion Aquitaine and INRA, and was under-
taken within the Labex COTE research project. We thank Mrs.
Lucette Dufour and Mrs. Bernadette Darchen from Le Rucher du
Pe
´rigord (Dordogne), the Groupement de De
´fense Sanitaire des Ab-
eilles de Gironde (GDSA 33), Mr. Benjamin Viry (Andernos envi-
ronmental services), Mr. Eric Savary (SARL Arbres et Fore
ˆts
Services) and Mr. Jacques Tardits. We are grateful to Dr. Olivier Le
Gall (scientific director of INRA) for encouraging this research by
providing organizational facilities and Dr. Hubert de Rochambeau for
allowing experimentation in the INRA Bordeaux-Aquitaine research
centre. We are also grateful to Dr. Phil Lester and three anonymous
reviewers for their help to improve the quality of our manuscript.
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