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ORIGINAL PAPER
Role of insect vectors in epidemiology and invasion risk
of Fusarium circinatum, and risk assessment of biological
control of invasive Pinus contorta
Eckehard G. Brockerhoff .Margaret Dick .
Rebecca Ganley .Alain Roques .
Andrew J. Storer
Received: 28 June 2015 / Accepted: 9 January 2016
ÓSpringer International Publishing Switzerland 2016
Abstract Pitch canker, caused by the pathogen
Fusarium circinatum, is a serious disease of pines,
Pinus species. It is a threat to natural and planted pine
forests, and to date it has invaded countries across five
continents. Pine-feeding insects can play a key role in
the epidemiology of the disease, as wounding agents
allowing pathogen access or as vectors transmitting
the pathogen from infected to healthy trees. We
reviewed the role of insects in the epidemiology of
pitch canker worldwide and assessed which insects are
present in New Zealand that may act as wounding
agents or vectors to determine whether pathogen
invasion could adversely affect Pinus radiata planta-
tion forests and urban trees. We also evaluated
whether cone or seed insects of pines could be
introduced as biological control agents of invasive
Pinus contorta and how this may affect the impact of a
potential F. circinatum invasion. As there are no
native pines or other Pinaceae in New Zealand, there
are only a few pine insects, mainly accidental intro-
ductions. None of the insects recorded on pines in New
Zealand is likely to be a vector, suggesting low disease
risk. Of six potentially suitable biocontrol candidates,
the European pine cone weevil Pissodes validirostris
is the most promising regarding host specificity and
impact on seed production, but there is uncertainty
about its ability to act as a vector of F. circinatum. Our
methodology to review and evaluate the vector
potential of pine associates can be used as a generic
framework to assess the potential impacts of F.
circinatum invasion.
Keywords Cone and seed insects Invasive alien
species Pathogen vectors Pitch canker
Electronic supplementary material The online version of
this article (doi:10.1007/s10530-016-1059-8) contains supple-
mentary material, which is available to authorized users.
E. G. Brockerhoff (&)
Scion (New Zealand Forest Research Institute),
Christchurch, New Zealand
e-mail: eckehard.brockerhoff@scionresearch.com
M. Dick R. Ganley
Scion (New Zealand Forest Research Institute), Rotorua,
New Zealand
e-mail: margaret.dick@scionresearch.com
R. Ganley
e-mail: rebecca.ganley@scionresearch.com
A. Roques
INRA – UR0633, Zoologie Forestie
`re, 2163 Av. Pomme
de pin, CS 40001, 45075 Orle
´ans, France
e-mail: alain.roques@orleans.inra.fr
A. J. Storer
School of Forest Resources and Environmental Science,
Michigan Technological University, 1400 Townsend
Drive, Houghton, MI 49931, USA
e-mail: storer@mtu.edu
123
Biol Invasions
DOI 10.1007/s10530-016-1059-8
Introduction
Pitch canker, caused by the pathogen Fusarium
circinatum (Nirenberg and O’Donnell), is a serious
disease of some pines (Pinus spp.) (Dick 1998;
Gordon et al. 2001; Wingfield et al. 2008). Since the
1980s it has emerged as a particularly damaging
disease of Pinus radiata D. Don in the native range of
this pine in various parts of California (Storer et al.
1997; Gordon et al. 2001). The pathogen is assumed to
originate from Mexico/Central America (Wingfield
et al. 2008) from where it has invaded the United
States, Haiti, Japan, South Africa, Chile, Spain, Brazil
and Italy, affecting a range of pine species (Dwinell
1999; Wingfield et al. 2002; Carlucci et al. 2007;
Wingfield et al. 2008; Pfenning et al. 2014). The extent
of disease problems varies among regions and host
species, and symptoms can be common in forests and
plantations (as in Spain, for example), restricted to
nurseries (as reported from Chile), or parks and
gardens (as in Italy). In South Africa, where pitch
canker was first detected in 1990 (Viljoen et al. 1994),
the disease remained confined to nurseries until 2005
when an outbreak was reported in young plantations in
the Western Cape Province (Coutinho et al. 2007).
Several countries where the disease has not yet been
recorded, including New Zealand, China, and Aus-
tralia, are thought to have a climate that is suitable for
establishment of the fungus and development of pitch
canker disease (Ganley et al. 2009).
Studies in California have shown that bark-feeding
insects as well as cone and seed insects play an
important role in the infection process, as wounding
agents of trees that may allow pathogen access or as
vectors of the pathogen from infected to healthy trees
(Fox et al. 1991; Hoover et al. 1996; Storer et al. 1998,
2004a). In New Zealand and other countries in the
southern hemisphere where Pinus radiata is widely
planted as an exotic tree, there are relatively few
associated insects, mainly because no native Pinaceae
are present, and consequently there are no native
specialised insect herbivores. Occasionally, some
native insects attack pines, although their direct
impact is mostly benign. However, several insect
pests of pines have become introduced over the years.
Preliminary reviews of the role of insects associated
with pines in New Zealand as potential vectors of F.
circinatum have been provided by Gadgil et al. (2003)
and Storer et al. (2004b). Currently, there appear to be
few insects in New Zealand that are likely to act as
vectors of the fungus, and this may limit the spread of
the fungus and its impact on pine plantations, if it ever
became established there. However, a formal analysis
of the potential vectors of F. circinatum in New
Zealand is not available.
Knowledge about any potential disease vectors and
other insect associates is necessary to enable an
informed response in the event of an incursion of F.
circinatum and to evaluate the risk of spread (Gadgil
et al. 2003; Ganley 2007; Fourrier et al. 2015). The
vector issue is also important for an assessment of the
risk of the potential intentional introduction of seed-
feeding insects for biological control of wilding
(invasive) Pinus contorta Loudon. Several pine
species are now considered environmental weeds in
New Zealand and other southern hemisphere countries
(Richardson and Higgins 1998; Rundel et al. 2014). In
some regions of New Zealand, pines have invaded
natural or semi-natural grassland and scrub commu-
nities (Ledgard 1998). Although plantings of Pinus
contorta were of limited extent, this species is now
considered the most serious invader among the pines
(Ledgard 1998). Options for biological control have
been assessed (Brockerhoff and Kay 1998; Brocker-
hoff et al. 2004). Because several pine species are
highly valued in plantation forestry and also in urban
amenity plantings, the potential use of cone and seed
insects is a favoured approach as such insects may
reduce the spread of pines without affecting growth or
causing damage to other parts of trees. In addition,
most cone and seed insects are specialised, adapted
species that exhibit a high degree of host plant
specificity (Turgeon et al. 1994), therefore limiting
risks to non-target plants. On the other hand, seed-
eating insects may not be as effective as other types of
biocontrol agents, and it remains to be determined
whether their effect actually reduces plant spread rates
(e.g., Rees and Paynter 1997). Based on a review of
cone and seed insects that attack Pinus contorta,
considering host specificity, potential impact on seed
production and other criteria, some insects are thought
to show promise as potential biocontrol agents, both in
New Zealand and South Africa (Brockerhoff and Kay
1998; Brockerhoff et al. 2004; Roques et al. 2004).
However, it is feared that the introduction of such
insects to New Zealand would greatly increase the
risks associated with F. circinatum because the
E. G. Brockerhoff et al.
123
biocontrol agent may act as an additional, and
potentially important, vector of the pitch canker
pathogen. In South Africa, such concerns have halted
plans to introduce a cone insect for biocontrol of
invasive pines (Lennox et al. 2009), although there is
renewed interest in the approach.
Here we review the role of insects in the epidemi-
ology of pitch canker world-wide and assess which
insects present in New Zealand may act as vectors. We
also review the preliminary selection of biocontrol
agents against invasive pines and explore the risks of
introducing such biocontrol agents to New Zealand,
particularly with regard to our current knowledge
about implications for vectoring F. circinatum. Our
specific objectives are:
1. to provide an overview of the insects associated
with pitch canker and their role in disease
epidemiology in the countries where the disease
occurs to date;
2. to review the native and introduced insects found
on pines in New Zealand, to determine the
likelihood of these species acting as vectors of
F. circinatum;
3. to evaluate the insects potentially suitable for
biocontrol of Pinus contorta in New Zealand and
to assess the risk of their introduction in relation to
the potential establishment of F. circinatum; and
4. to develop a general framework for the assessment
of risks associated with vectors of F. circinatum or
similar pathogens that can also be used for other
countries.
Wounding agents, vectors and carriers of Fusarium
circinatum and their interactions with the pathogen
In some regions insects have been shown to play an
important role in the infection process while in other
regions insects appear to play a minor role. Associ-
ations with insects have been best studied in California
where pitch canker has become a major disease of the
native Pinus radiata, which is among the most
susceptible species of pine (Correll et al. 1991; Adams
et al. 1999; Storer et al. 2002). Insects can act as
‘wounding agents’ that allow the pathogen to enter the
plant via the damaged cuticle or via tunnels such as
those made by bark beetles. Some insects are ‘carriers’
because they carry inoculum from diseased plants they
either visited or on which they have developed.
However, in order to be classified as a ‘vector’,
Leach’s postulates need to be met (Leach 1940). These
state that in addition to being associated with diseased
plants, carrying the pathogen, and visiting susceptible
plant hosts, an organism must be capable of success-
fully transmitting the pathogen to plants that were not
yet infected under controlled conditions. Some
wounding agents act concurrently as vectors but a
vector can also cause an infection via a wound caused
by another species. Not all carriers of inoculum are
necessarily successful vectors, for example, if they are
not causing any wounding that would be sufficient for
transmission. It is therefore important to consider the
differences in involvement of the various insects
associated with diseased or healthy host plants and to
classify each species accordingly (Table 1).
Insects that feed subcortically on live trees or that
wound live trees during exploratory host feeding have
been shown to vector the pitch canker pathogen in
California, especially bark beetles such as Ips para-
confusus (Fox et al. 1991) and twig beetles, Pityoph-
thorus spp. (Storer et al. 2004a; Erbilgin et al. 2008;
Table 1; see Supplementary Table S1 for an alpha-
betical listing of insect species). Twig beetles are
thought to vector the pitch canker pathogen into pines
also during exploratory feeding to find suitable host
material. Baiting trees with pheromones of Pityoph-
thorus setosus resulted in pitch canker infections on
those trees despite the lack of colonization by the
insect (Storer et al. 2004a). Other habits that may
result in wounding include shoot feeding and the
creation of wounds during oviposition. The cone-
infesting beetles, Conophthorus radiatae and Erno-
bius punctulatus are also confirmed vectors (Hoover
et al. 1995,1996; Table 1). Several other species,
including shoot and foliage feeders, sap suckers and
predatory insects are known wounding agents or
carriers but none of these are known vectors (Table 1,
Supplementary Table S1).
To assess the role of insects in the infection of trees
by F. circinatum and the epidemiology of the disease,
it is important to consider the life cycles of both the
pathogen and potential vectors and the nature of
potential interactions between these organisms. Fruit
bodies of F. circinatum (known as sporodochia)
containing thousands of asexual spores (conidia)
may be produced on the surface of infected tissues
when conditions are moist. These are dispersed by
Role of insect vectors in epidemiology and invasion risk of Fusarium circinatum
123
Table 1 Insects associated with Fusarium circinatum in regions where pitch canker occurs and the nature of their association
Species (*non-indigenous sp.) Order, family
(subfamily)
Wounding
agent
a
Carrier
a
Confirmed
vector
a
References
USA (South-East)
Bark beetles and wood borers
Pissodes nemorensis Col., Curculionidae, Molytinae ?? Blakeslee et al. (1978),
Blakeslee and Foltz
(1981)
Shoot and foliage-feeders
Rhyacionia spp. Lepidoptera, Tortricidae ?Matthews (1962)
Contarinia spp. Diptera, Cecidomyiidae ?Dwinell et al. (1985)
Cone insects
Cydia spp. Lepidoptera, Tortricidae ?Dwinell et al. (1985)
Leptoglossus corculus Heteroptera, Coreidae ?Dwinell et al. (1985)
USA (California)
Bark beetles and wood borers
Ips paraconfusus Col., Curculionidae, Scolytinae ???Fox et al. (1991)
Ips mexicanus, Col., Curculionidae, Scolytinae (?)?(?) Fox et al. (1991), Erbilgin
et al. (2008)
Ips plastographus
maritimus
Col., Curculionidae, Scolytinae (?)?(?) Fox et al. (1991), Erbilgin
et al. (2008)
Pityophthorus setosus Col., Curculionidae, Scolytinae ???Hoover et al. (1995), Storer
et al. (2004a), Erbilgin
et al. (2005)
Pityophthorus carmeli Col., Curculionidae, Scolytinae ??(?) Hoover et al. 1995), Storer
et al. (2004a), Erbilgin
et al. (2005)
Hylastes spp. Col., Curculionidae, Scolytinae (?)?Storer et al. (2004b)
Hylurgops spp. Col., Curculionidae, Scolytinae (?)?Storer et al. (2004b)
Dendroctonus valens Col., Curculionidae, Scolytinae (?)?Storer et al. (2004b)
Pissodes radiatae Col., Curculionidae, Molytinae? (?)?Storer et al. (2004b)
Sapsuckers
Aphrophora canadensis Homoptera, Cercopidae ?Storer et al. (1998)
Shoot and foliage-feeders
(none)
Cone insects
Conophthorus radiatae Col., Curculionidae, Scolytinae ???Hoover et al. (1995,1996)
Ernobius punctulatus Col., Anobiidae ?? Hoover et al. (1995,1996)
Predatory insects
Enoclerus sphegeus Col., Cleridae ?Dallara (1997), Storer et al.
(2004b)
Lasconotus spp. Col., Colydiidae ?Dallara 1997), Storer et al.
(2004b)
Medetera spp. Dipt: Dolychopodidae ?Storer et al. (2004b)
Non-insect taxa
Snails and Pillbugs/
Sowbugs
Mollusca and Crustacea
(Isopoda)
?Storer et al. (2004b)
South Africa
Shoot and foliage-feeders
E. G. Brockerhoff et al.
123
water-splash and can be carried in air currents
throughout the year (Blakeslee et al. 1978; Correll
et al. 1991). Spores can also be recovered from the
surface bark of trees even when fruit bodies are not
readily apparent (Adams et al. 1999). Two rounds of
studies have been conducted where spore suspensions
were sprayed on small trees in the field and the
branches were then baited with twig beetle phero-
mones (Sakamoto et al. 2007). The results showed no
difference in disease between treated and untreated
trees. It is likely that spore loads were very high in
these studies compared with what occurs naturally. It
seems likely that the insects pick up spores in the tree,
perhaps while chewing their way out though diseased
tissue. Insects coming into contact with the sporodo-
chia may readily pick up many of the sticky spores that
are likely to adhere to the surface of the body and be
trapped amongst hairs and other surface structures
(e.g., Yamoah et al. 2011). Fox et al. (1990) reported
the isolation of the pathogen from galleries of Ips spp.
in Pinus radiata trees. The beetles carry propagules
that presumably can include hyphal fragments as well
as spores. By contrast, it is likely that the importance
of casually acquiring spores from the tree surface is
low. The risk of transmission appears to vary at
different times of the year according to propagule
loads on two Ips species (Erbilgin et al. 2008). Spore
loads of twig beetles were considered an important
factor in studies of the vector efficiency (Erbilgin et al.
2009).
Once infection has occurred the fungus colonises
the sapwood and can be readily isolated from
discoloured or resinous tissues (McCain et al. 1987;
Correll et al. 1991). However, the fungus does not
Table 1 continued
Species (*non-indigenous sp.) Order, family
(subfamily)
Wounding
agent
a
Carrier
a
Confirmed
vector
a
References
Pissodes sp.* Col., Curculionidae, Molytinae (?) (?) (?) Coutinho et al. (2007)
Bradysia difformis Diptera, Sciaridae (?) Hurley et al. (2007)
Chile
Bark beetles and wood borers
Hylastes ater* Col., Curculionidae, Scolytinae (?) Wingfield et al. (2008)
Japan
None (?, see text) Viljoen et al. (1997)
Spain
Bark beetles and wood borers
Hylastes attenuatus Col., Curculionidae, Scolytinae (?)?Romo
´n et al. (2007)
Hylurgops palliatus Col., Curculionidae, Scolytinae (?)?Romo
´n et al. (2007)
Hypothenemus eruditus Col., Curculionidae, Scolytinae (?)?Romo
´n et al. (2007)
Ips sexdentatus Col., Curculionidae, Scolytinae (?)?Romo
´n et al. (2007)
Orthotomicus erosus Col., Curculionidae, Scolytinae (?)?Romo
´n et al. (2007)
Pissodes castaneus Col., Curculionidae, Molytinae (?)?Iturritxa et al. (2011)
Pityophthorus pubescens Col., Curculionidae, Scolytinae (?)?Romo
´n et al. (2007),
Iturritxa et al. (2011)
Tomicus piniperda Col., Curculionidae, Scolytinae (?)?Iturritxa et al. (2011)
Cone insects
Pissodes validirostris Col., Curculionidae, Molytinae ?(?) Roques et al. (2004),
Lennox et al. (2009)
Root borers
Brachyderes incanus Col., Curculionidae, Entiminae (?)?Romo
´n et al. (2007)
See Supplementary Table S1 for an alphabetical listing of insect species
a
Nature of association: ?, confirmed association; (?), presumed association not yet verified; (?), suspected but less likely or
unknown association (for details see text)
Role of insect vectors in epidemiology and invasion risk of Fusarium circinatum
123
spread great distances within the wood. Infection of a
cone, or a cone whorl, vectored by cone insects or
other borers leads to death of the branch beyond the
cone, with each dead branch being the result of a
separate infection. Although unsightly, the branch and
twig death that would result from infections transmit-
ted by cone and seed insects would probably have
relatively little impact on tree growth. Lesions on
branches girdle the branch so the distal portion dies;
spread down the branch or shoot is usually arrested at
the node (Dwinell et al. 1985; Gordon et al. 2001).
Individual trees may thus sustain crown infections for
many years. However, crown dieback can be extensive
due to the multiple infections. Trunk infections are
often initiated by bark beetles, and tree death will
follow girdling of the stem from a number of separate
infections and/or attacks by bark beetles. Multiple
trunk attacks are required in order to kill the cambium
around the circumference and for tree death to result
(Gordon et al. 2001; Storer et al. 2002). Bark beetles
(especially Ips spp. and Dendroctonus spp.) can cause
considerable mortality of pines also in the absence of
any other disease agents (e.g., Six and Wingfield
2011).
In the absence of insects vectoring F. circinatum to
the trunk of the trees, any stem infections would be
initiated through infection of wounds created by other
causes including weather events (such as wind and
hail), pruning or cone collection (Dwinell et al. 1985;
Gordon et al. 2001). In New Zealand, wounds could
also occur from bark stripping by native parrots (Dick
1998), although this is rare.
Spread of the pitch canker disease in nurseries is
different from what occurs in forests. The fungus has
been reported to be capable of spreading through
nurseries very rapidly, with devastating losses
recorded (Viljoen et al. 1994). Unlike in older trees,
wounds are not required for infection of young
seedlings. Insect-vectored transmission is apparently
not important (Hurley et al. 2007). Unfortunately, in
contrast to the majority of pine nursery diseases where
diligent application of fungicides will generally
reduce the impacts of pathogens, chemical control of
pitch canker disease has been found to be relatively
ineffective (M.J. Wingfield pers. com.). However,
rigorous sanitation procedures can reduce disease
incidence to insignificant levels in a nursery where all
plants are containerised (Van Wyk et al. 2012). Based
on this knowledge, we can predict with reasonable
confidence the outcome of an introduction of F.
circinatum to a nursery in New Zealand where plants
are reared both as bare root in nursery beds and in
containers (Gadgil et al. 2003). Eradication attempts
are likely to result in nursery closure while soil
fumigation is undertaken followed by a high level of
sanitation. Although insects are not thought to be
important in the disease epidemiology within nurs-
eries, certain insects may be involved in spreading the
disease from nurseries to surrounding forests. It is
more likely that transmission of the fungus to a
plantation would occur via out planting of asymp-
tomatic infected seedlings from a nursery than by
insects.
Potential vectors present in New Zealand
Where pines occur naturally there is a substantial
fauna of associated insects. For example, in North
America (north of Mexico) over 1100 insect species
have been recorded as feeding on pines, including
about 30 introduced insect species (de Groot and
Turgeon 1998). The majority of these species were
classed as either monophagous (ca. 50 %) or oligo-
phagous (ca. 30 %) (i.e., more or less specific to
pines).
The New Zealand flora includes no native pines or
any other native Pinaceae, and as a result there are no
native insects that are closely associated with pines.
However, several native insects, primarily polypha-
gous species, have colonised pines growing in New
Zealand, usually occurring at low densities (e.g.,
Berndt et al. 2004). The most common insects found
on pines in New Zealand are introduced species from
the native range of pines, mainly from Europe and
North America, such as a number of bark beetles and
longhorned beetles (Brockerhoff et al. 2006).
To obtain an indication of the relative abundance of
insects associated with pines in New Zealand we
queried the Forest Health Database (maintained by
Scion/New Zealand Forest Research Institute) (Bul-
man 1990). The database of forest health surveillance
reports contains over 3000 records of formally iden-
tified insects. This provided a list of over 500 insect
species although most of these represent incidental
observations of species that do not feed on pines.
Nevertheless, the results of this database query do
reflect which pine-feeding insects are most commonly
E. G. Brockerhoff et al.
123
found on pines growing in New Zealand’s plantation
forests and as amenity trees. These common associates
are most likely to play a role in the epidemiology of the
pitch canker disease, should it become established in
New Zealand. By contrast, insects that are only rarely
found on pines are probably irrelevant, especially if
they have no feeding or other close relationship. The
25 most commonly recorded insect species on pines in
New Zealand (Table 2) represent all the feeding guilds
of insects that have been considered overseas with
regard to their association with pitch canker, except
for pine cone insects (of which there are none in New
Zealand except for the rarely found Erechthias fulgu-
ritella which does not normally attack pine cones), and
predators or parasitoids (of which several were
recorded but at low frequencies). These common
associates were categorised with regard to the host
status during attack (i.e., live or dead trees) using
information from Scion’s Forest Health Database and
from the Forest and Timber Insects series (e.g.,
Brockerhoff and Hosking 2001). All species were
then assessed for their potential to act as a wounding
agent, carrier of F. circinatum inoculum, or vector
(Table 2).
Currently there are no high-risk species in New
Zealand that could act as a vector of the pitch canker
pathogen. Of the insect species that have been
demonstrated to vector F. circinatum elsewhere, none
are currently known to exist in New Zealand. Ernobius
mollis, an alien anobiid, is the only species that occurs
in New Zealand that has a congeneric species known
to vector the pathogen in the United States. Ernobius
mollis colonises and breeds mostly in dead trees and it
is therefore unlikely to be able to vector the pathogen
to live trees although it has occasionally been observed
in Europe to colonize cones of Pinus brutia, Pseudot-
suga menziesii and Sequaiodendron gigantea attacked
by cone pyralids (Roques 1983). Of the insects that
have been recorded from Pinus radiata in New
Zealand, it is those that feed subcortically on live
trees or that wound live trees during exploratory host
feeding (such as Ips paraconfusus and Pityophthorus
setosus in California) that would represent the greatest
concern regarding association with the pitch canker
pathogen. No such species that is a confirmed vector is
present in New Zealand (Table 2). Of the other
species, Hylastes ater is a representative of a genus
that is known to carry the pathogen in the United States
(Storer et al. 2004b). In Spain, F. circinatum has not
been isolated from H. ater, however, another species
in the same genus, Hylastes attenuatus, can be a carrier
of the pathogen (Romo
´n et al. 2007,2008). Neverthe-
less, Hylastes ater is known to attack seedlings (for
maturation feeding) and this could raise its risk status
but based on current information, it is not thought to be
a potential vector. Sirex noctilio is known to attack live
pine trees but for several decades the species has been
generally uncommon in New Zealand (Bain et al.
2011). Furthermore, it is not known to be a carrier of F.
circinatum in any country where pitch canker occurs.
Therefore, it is unlikely to become an important vector
if F. circinatum became established in New Zealand.
Gadgil et al. (2003) list 14 sap-feeding species as
potential vectors of the pitch canker pathogen in New
Zealand, although most of these are not associated
with pines. Among sap feeding species in California,
only spittlebugs have been shown to be associated
with pitch canker (Storer et al. 1998), even though
other sap feeding species such as the Monterey pine
scale, Physokermes insignicola (Homoptera: Cocci-
dae), commonly occur in native and planted Pinus
radiata forests in California. The absence of a
spittlebug feeding on Pinus radiata in New Zealand
and the apparent lack of association of the pathogen
with other sap feeders suggests that these species
should not be considered to be significant associates of
F. circinatum in New Zealand.
Potential biological control agents for invasive
pines
A preliminary evaluation of potential biological
control agents against wilding pines in New Zealand
was conducted by Brockerhoff and Kay (1998). The
main target species was Pinus contorta because it is
considered the most important invader. Also, this pine
has not been planted in commercial plantations for
several decades, and biocontrol using seed-feeding
insects is therefore less controversial than against a
target species that is economically important (Brock-
erhoff and Kay 1998). A number of criteria were
applied in the selection of potential agents including:
the candidate agent should have a host range that
includes the target species and subspecies, be suffi-
ciently host specific such that it would not attack non-
target tree species, be compatible with the climate in
the target region(s) in New Zealand, reduce seed
Role of insect vectors in epidemiology and invasion risk of Fusarium circinatum
123
production of the target species substantially, and be
able to disperse to isolated tree populations. In
addition, the agent should not have any other
unwanted effects such as a potential contribution to
tree disease dynamics (see below). The survey
focussed on cone insects within the natural range of
Table 2 Insects present in New Zealand that may act as associates with Fusarium circinatum
Species (* non-
indigenous sp.)
Family (subfamily) Origin (native
region)
Attacks live (L) or dead
plants (D)
a
Potential pitch canker
association
b
Bark beetles and wood borers
Hylastes ater* Curculionidae, Scolytinae Europe (L)
a
DW,C
Hylurgus ligniperda* Curculionidae, Scolytinae Europe D C
Pachycotes peregrinus Curculionidae, Scolytinae NZ D C
Platypus apicalis Curculionidae,
Platypodinae
NZ D C
Arhopalus ferus* Cerambycidae Europe (L)
a
D (W), C
Calliprason pallidus Cerambycidae NZ D C
Hexatricha
pulverulenta
Cerambycidae NZ (L)
a
DC
Oemona hirta Cerambycidae NZ (L)
a
D (W), (C)
Prionoplus reticularis Cerambycidae NZ D C
Ernobius mollis* Anobiidae Cosmopolitan D C
Sirex noctilio* Siricidae Europe L C
Mitrastethus
baridioides
Curculionidae,
Cryptorhynchinae
NZ D (C)
Pycnomerus sophorae Colydiidae NZ D (C)
Shoot and foliage-feeders
Pseudocoremia suavis Geometridae NZ L W, (C)
Hierodoris
atychioides
Oecophoridae NZ L W, (C)
Ctenopseustis
obliquana
Tortricidae NZ L W, (C)
Epiphyas postvittana* Tortricidae Australia L W, (C)
Planotortrix
notophaea
Tortricidae NZ L W, (C)
Sapsuckers
Pineus boerneri* Adelgidae USA L (W), (C)
P. pini* Adelgidae Europe L (W), (C)
Essigella californica* Aphididae USA L (W), (C)
Eulachnus
brevipilosus*
Aphididae Europe L (W), (C)
Heliothrips
haemorrhoidalis*
Thripidae Cosmopolitan? L (W), (C)
Cone insects
Erechthias fulguritella Tineidae NZ (?) (?)
a
Hylates ater sometimes attacks pine seedlings for maturation feeding; Arhopalus ferus has been recorded as attacking live trees but
this is rare and probably limited to fire-damaged trees; Hexatricha pulverulenta sometimes breeds in pines, always dead trees, but
occasionally it feeds on green twigs of pine (Bain and Hosking 1988); Oemona hirta is normally associated with hardwood trees and
attacks of softwoods are very rare (Hosking 1978)
b
Possible association in case of establishment of F. circinatum in New Zealand: Wwounding agent of live trees, Ccarrier, Vvector;
values in brackets indicate uncertainty of association; (see text for details)
E. G. Brockerhoff et al.
123
Pinus contorta and also on cone insects that have
colonised the species in areas where the tree was
introduced, especially in parts of Europe. Based on
this, 16 species were assessed (Brockerhoff and Kay
1998) of which six species were considered to be
potentially suitable and worthy of further considera-
tion and research (Table 3). The other species were
insufficiently host specific or attacked other parts of
trees, which could affect tree growth.
The North American cone moth Eucosma rescis-
soriana can significantly reduce seed production, but
this species was disregarded on the basis of its wider
host range that covers firs (Abies grandis,A. lasio-
carpa) and pines (Pinus contorta,Pinus monticola and
possibly Pinus albicaulis; Hedlin et al., 1980). How-
ever, the host range of this species should be reviewed
as all other species of Eucosma are genus-specific, and
it is unusual that Eucosma rescissoriana attacks both
firs and pines. Three other species, the anobiid
Ernobius nigrans, the cerambycid Paratimia conicola,
and the tortricid Cydia toreuta, may be sufficiently
host specific but they usually have a more limited
effect on seed production, at least in their natural
geographic range. Most promising were the pine cone
beetle Conophthorus ponderosae, a North American
species, and Pissodes validirostris, the European pine
cone weevil. Both these species have a narrow host
range and the ability to reduce seed production
considerably (Brockerhoff and Kay 1998; Brockerhoff
et al. 2004). However, Pissodes validirostris appeared
to be the most effective in terms of its effects on seed
production, possibly because the two species did not
co-evolve, and Pinus contorta may not have devel-
oped adaptations against this particular cone
insect. Based on these findings, we prioritised Pis-
sodes validirostris as the agent of first choice for more
detailed consideration and for potential introduction to
New Zealand.
Out of a total of 21 insect species known to develop
in the cones of Pinus spp. in Europe and in the
Mediterranean basin, Pissodes validirostris is the most
damaging cone insect (Roques 1983; Roques and El
Alaoui El Fels 2002). Most other species cause only
minor damage. Pissodes validirostris is present all
over the Palaearctic region from Portugal and Scan-
dinavia to northern China (Roques 1983). Larvae of
Pissodes validirostris develop exclusively in pine
cones, tunneling through the tissues and destroying the
seeds. They attack native pines of the subgenus Pinus
such as Pinus sylvestris,P. mugo,P. uncinata,P. nigra
and subspecies, and P. leucodermis which all belong
to the subsection Pinus (Gernandt et al. 2005), as well
as Mediterranean pines of the subsection Pinaster,
such as P. pinaster,P. halepensis, and P. pinea)
(Roques, 1983). Weevil attacks are also recorded on
some North American pines widely planted in Europe
Table 3 Most promising candidate agents for biocontrol of Pinus contorta in New Zealand
a
, their characteristics, and potential for
involvement with the pitch canker disease
Species Family
(subfamily)
Host range
b
Host structures
attacked
Potential pitch canker
association
e
Coleoptera
Conophthorus ponderosae Curculionidae Pinus spp., not P. radiata Only seed cones W, C, (V)
Ernobius nigrans Anobiidae Pinus spp., not P. radiata Only seed cones W, C, (V)
Paratimia conicola Cerambycidae Pinus spp., not P. radiata Only seed cones W, C, (V)
Pissodes validirostris Curculionidae Pinus spp., not P. radiata
c
Mainly seed cones
d
W, C, (V)
Lepidoptera
Cydia toreuta Tortricidae Pinus spp., not P. radiata Only seed cones W, C, (V?)
Eucosma rescissoriana Tortricidae Pinus and Abies spp., not P. radiata Only seed cones W, C, (V?)
a
Preliminary selection of potential agents according to Brockerhoff and Kay (1998) and Brockerhoff et al. (2004)
b
Host range information based on Keen (1958), Hedlin et al. (1980) and other publications listed in Brockerhoff and Kay (1998)
c
Depending on the subspecies/host race of P. validirostris (see text)
d
Maturation feeding, apparently causing little damage, occurs on shoots (see text)
e
Possible association in case of establishment of Fusarium circinatum in New Zealand: Wwounding agent of live trees, Ccarrier,
Vvector; values in brackets indicate uncertainty of association; (for details see text)
Role of insect vectors in epidemiology and invasion risk of Fusarium circinatum
123
such as lodgepole pine, Pinus contorta (Annila 1975;
Delplanque et al. 1988), a species of the subgenus
Pinus but from the section Trifoliae. Cone damage
from P. validirostris was recently noticed in French
arboreta on Pinus hartwegii (=P. rudis), a member of
the subsection Ponderosae (Alain Roques, unpub-
lished data). By contrast, the North American pines
Pinus radiata and P. taeda, belonging to the subsec-
tion Australes of the subgenus Pinus, are not known to
be attacked or damaged, despite the presence of large
areas of planted forest of these species in parts of
south-western Europe where Pissodes validirostris is
generally very common on its normal hosts (Roques
et al. 2004). In addition, native pine species in the
subgenus Strobus such as Swiss stone pine (Pinus
cembra), are avoided (Dormont and Roques 1999)as
are exotic pines of the same subgenus, probably due to
specific host volatiles (Dormont and Roques 2001).
However, host-specificity tests revealed that there are
different biotypes of P. validirostris which specialize
on pines either of the subsection Pinus or of the
subsection Pinaster (Roques et al. 2004). Recent
molecular and morphometric studies confirmed that
the species Pissodes validirostris probably incorpo-
rates discrete taxa, or at least independent evolution-
ary lineages. At least three phylogeographic lineages
were identified corresponding to the populations of the
Iberian Peninsula, Central Europe and Northern/East-
ern Europe, respectively, which correspond to the
differences in host plant preferences (Ge
´raldine Roux,
pers. comm.). Populations that colonized Pinus con-
torta are more closely associated with Central and
Northern European populations on P. sylvestris than
with those developing on Mediterranean pines (Ro-
ques et al. 2004;Ge
´raldine Roux, pers. comm.). This
suggests that P. sylvestris was the original host for
these populations. In no-choice host selection exper-
iments, both biotypes of Pissodes were capable of
laying eggs on cones of Pinus radiata, but only the
larvae originating from populations of the P. sylvestris
biotype were capable of completing their development
in these cones (Roques et al. 2004).
Cone damage by Pissodes validirostris greater than
80 % has been reported from natural stands of Pinus
pinea in Spain (Bachiller 1966) and of P. sylvestris
and Pinus uncinata in France (Roques 1977; Roques
et al. 1983). However, Pinus contorta appears to be
significantly more attacked than P. sylvestris when
these two species are planted in proximity. In Finland,
42–94 % of Pinus contorta cones were damaged by
Pissodes validirostris compared with 1–55 % of P.
sylvestris (Annila and Hiltunen 1977). In central
France, cone damage in Pinus contorta was nearly
twice the damage in P. sylvestris (82.0 vs. 46.3 %)
(Delplanque et al. 1988). Larvae of Pissodes validir-
ostris affect seed yield by direct feeding and by
inducing resin bleeding (Roques 1976). Resin bleed-
ing reduces seed dispersal by preventing the cone
scales from opening (Roques 1976). In P. sylvestris,
3–4 larvae of P. validirostris are enough to destroy a
cone completely (Roques 1976), but in pine species
with larger cones (e.g., Pinus pinaster) the number of
larvae must be greater than four to get the same result.
In the small-sized cones of Pinus contorta, each
weevil larva is responsible for a loss of 40 to 60 % of
the seed content (Delplanque et al. 1988) whilst the
presence of two larvae per cone increases seed loss to
ca. 80 % (Annila 1975).
Risks associated with introducing biocontrol agents
against invasive pines
Based on the available information about potential
effectiveness and non-target impacts, the most
promising potential biocontrol agents against wild-
ing pines in New Zealand are the ponderosa pine
cone beetle, Conophthorus ponderosae, and the pine
cone weevil, Pissodes validirostris (Brockerhoff and
Kay 1998, above). In addition, the lodgepole pine
cone moth, Eucosma rescissoriana, could be con-
sidered if it can be determined that it is sufficiently
host specific. There are important issues that need to
be addressed concerning the risk of these insects
becoming vectors of the pitch canker pathogen and
thereby causing unwanted damage of pines in
planted forests. Biocontrol agents that enter the host
tissues (as opposed to feeding externally) have a
high potential to act as vectors of the pitch canker
pathogen. In addition, those that cause wounds to
branches and stems may also act as vectors as has
been shown for twig beetles in the western United
States (e.g. Storer et al. 2004a).
Conophthorus ponderosae has a congeneric species
that is a confirmed vector of the pathogen in California
and therefore it may be a vector in New Zealand.
Although Pinus radiata is not a known host species
(Storer et al. 2004b), a host switch could occur.
E. G. Brockerhoff et al.
123
The lodgepole pine cone moth, Eucosma rescisso-
riana, may become associated with the pitch canker
pathogen as a vector or as a wounding agent. A shift in
habit by this species to include the shoot feeding habit
exhibited by other members of the genus could also
increase the significance of any association with the
pathogen.
Although larval and pupal development of Pissodes
validirostris occurs entirely in seed cones, adult
weevils require maturation feeding, typically on the
pine leader shoots, in spring in order to become
sexually mature and capable of laying eggs on cones
(Roques 1976). Another period of feeding on leader
shoots is observed in autumn before the adults settle to
overwinter in the bark of the trees (Roques et al. 2004).
In contrast to egg-laying, behavioral tests showed that
the different biotypes of Pissodes validirostris can
feed on the shoots of a large number of pine species.
Such damage did not appear to affect plant health
(Roques et al. 2004), but it may help fungal transmis-
sion. Fresh adults washed immediately after emer-
gence from the cones did not carry any F. circinatum
conidia (Lennox et al. 2009). In an experiment,
feeding on Pinus radiata seedlings by adult P.
validirostria that had been artificially infested with
F. circinatum did not show any transmission of
conidia. However, its feeding damage appeared to
facilitate the ingress of the fungus into the host plant
(Lennox et al. 2009).
Based on these findings, it cannot be ruled out
that Pissodes validirostris, if it were introduced to
New Zealand, could act as a vector of F. circinatum
should the pathogen become established there. The
behavior of this species would allow several types
of association with the pitch canker pathogen
including spreading the pathogen by dissemination
through adults emerging with the pathogen, inocu-
lation of the pathogen during egg laying and adult
feeding, ingression through egg laying, adult and
larval feeding, and invasion during larval feeding.
The most likely responsible mechanism is the
maturation feeding behaviour of this weevil. Fur-
thermore, Pissodes validirostris has a demonstrated
ability to colonise new hosts, such as Pinus
contorta, and this represents a new insect-host plant
association. The potential for additional changes in
host use in new environments cannot be ruled out. If
Pissodes validirostris were to colonise and damage
cones of Pinus radiata, then it could also affect
breeding programmes and the production of seed for
nurseries.
Conclusions
The pitch canker disease caused by the pathogen F.
circinatum represents a major threat to pine forests
worldwide. Pinus radiata is one of the most suscep-
tible pines, and it is an important tree in planted forests
in New Zealand and several other countries where F.
circinatum does not yet occur. In New Zealand, this
risk is moderated by the fact that no known vectors of
F. circinatum are present. Our review identified
several species that could play a role in the epidemi-
ology of the disease in New Zealand, as wounding
agents or carriers of the pathogen, but no insects
appear to be present that could act as effective vectors.
Against this background, the proposed introduction of
biocontrol agents against invasive Pinus contorta or
other pines has been deemed too risky, mainly because
of the pitch canker pathogen vectoring issue (Dick and
Bain 2004). Furthermore, it is not certain how
effective a biocontrol agent would be in terms of
reducing the spread of wilding pines. While the
success of past biocontrol introductions has been high,
with 83 % providing partial or complete control of
target plants, seed eating agents have perhaps been
less effective (Fowler et al. 2000; Suckling 2013). A
similar proposal to introduce seed eating insects for
the control of invasive pines has been considered in
South Africa (Hoffmann et al. 2011). Recently it has
been decided not to pursue this further due to risks
associated with pitch canker in South Africa where the
disease is already present, and because of questions
about the effectiveness of biocontrol relying solely on
cone and seed insects (Lennox et al. 2009). Further
research on insects present in New Zealand and on
potential biocontrol agents could be conducted in
regions where these species occur and where F.
circinatum is also present (e.g., Spain and South
Africa for some of the European insects). This would
assist with further risk assessments and possible future
incursion responses.
Acknowledgments We thank John Bain for reviewing an
earlier version of the manuscript. Funding for this review was
obtained from the New Zealand Government (FRST contract
C04X0302 and Better Border Biosecurity via MBIE core
funding to Scion, contract C04X1104).
Role of insect vectors in epidemiology and invasion risk of Fusarium circinatum
123
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