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N E W P E R S P E C T I V E S
New Perspectives is intended to allow the communication of comments, viewpoints, and speculative interpretation of issues in
ecology pertinent to entomology. Comments, viewpoints, or suggestions arising from published papers intended to fuel discussion
and debate are also welcome. Contributions should be as concise as possible, normally not exceeding two thousand words. Formal
research reports will not be acceptable, but summarised novel data, suitably supported by statistics, may be allowed.
Modi®cation of coevolved insect±plant interactions byan exotic plant pathogen
A N D R E W J . S T O R E R , D A V I D L . W O O D and
T H O M A S R . G O R D O N *Division of Insect Biology, University of California, Berkeley, U.S.A. and
*Department of Plant Pathology, University of California, Davis, U.S.A.
Key words. Ecological interaction, Fusarium subglutinans, insect±plant
interactions, Monterey pine, pitch canker disease, Scolytidae, tree disease.
Introduction
Introductions of exotic tree pathogens have often had signi®cant
effects on forest communities. Prominent examples include
Cryphonectria parasitica (Murrill) M. E. Barr, the cause of
chestnut blight, which has effectively eliminated the native
American chestnut, Castanea dentata (Marsh.) Borkh., as a
dominant tree in eastern hardwood forests (Stephenson, 1986),
and Cronartium ribicola Fisch., the cause of white pine blister
rust, which has altered the species composition of western
coniferous forests (Byler et al., 1994). In addition to direct
effects on plant hosts, introduced pathogens can have indirect
effects on other organisms associated with the pathogen and/or
the host. For example, the invasion of a new habitat by a
microbe may be facilitated greatly by insect vectors. The
association between Ophiostoma novo-ulmi Brasier, the cause
of Dutch elm disease, and elm bark beetles, Scolytus spp., is
perhaps the best illustration of the potential for new associations
to in¯uence the evolutionary fate of insect, fungus, and tree
species simultaneously (Wing®eld et al., 1993). Plant pathogens
have the potential to alter signi®cantly the population size of
herbivorous insects (Hatcher, 1995) and other organisms
associated directly or indirectly with these insects.
The categorisation of an ecological interaction as, for
example, mutualistic or commensalistic, may be somewhat
restrictive in considering the versatility in the associations. To
avoid this, concise descriptions of ecological interactions and
indications of general positive, negative, and neutral effects in
these interactions are used here.
Changes in ecological interactions among insects and
Monterey pine (P. radiata D. Don) have resulted from the
introduction into California of Fusarium subglutinans
(Wollenweb. & Reinking) P. E. Nelson, Toussoun & Marasas
f. sp. pini (Correll et al., 1991) (Syn. F. moniliforme var.
subglutinans), the causal agent of pitch canker disease. This
disease was ®rst identi®ed in California in 1986, and was
found to be associated with the extensive mortality of planted
Monterey pines (McCain et al., 1987). The pitch canker
pathogen has apparently established new associations with
numerous native insect species that feed on Monterey pine, and
these have been shown to vector the pathogen (Fox & Schultz,
1991; Fox et al., 1991; Hoover et al., 1996). Insects are
believed to be responsible for initiating most of the infections
on pines in California. Mechanical wounding without arti®cial
inoculation has not resulted in the pitch canker infections of
cones (Correll et al., 1991) or branches (Fox et al., 1991).
The epidemiology of pitch canker in California has been
described in detail elsewhere (Storer et al., 1994; 1995a,b,
1997) and is summarised only brie¯y here. The ®rst symptoms
of the disease are usually branch tip die-back, resulting from
girdling lesions. These lesions are attributed to infections
caused primarily by the feeding activities of twig beetles
[Pityophthorus spp. (Coleoptera: Scolytidae)] (Fox & Schultz,
1991; Hoover et al., 1996), the Monterey pine cone beetle
[Conophthorus radiatae Hopkins (Coleoptera: Scolytidae)],
and a deathwatch beetle [Ernobius punctulatus Fall (Coleop-
tera: Anobiidae)] (Hoover et al., 1996). The disease intensi®es
due to repeated infections by the same mechanism. Bark beetles
[Ips spp. (Coleoptera: Scolytidae)] initiate pitch canker
infections on large branches and the main trunk (bole) of the
tree (Fox et al., 1991). The death of the entire tree often follows
the development of bole cankers. Thus, this exotic fungus may
L
Correspondence: Andrew J. Storer, Division of Insect
Biology, 201 Wellman Hall, Berkeley, CA 94720-3112, U.S.A.
E-mail: [email protected].
238 # 1999 Blackwell Science Ltd
Ecological Entomology (1999) 24, 238±243Ecological Entomology (1999) 24, 238±243
in¯uence the evolution of vector relationships between insects
and fungi, and promulgate changes in ecological interactions
among native insects cohabiting pines. While the magnitude of
these changes remains to be determined, the evidence to date
(e.g. Fox et al., 1990, 1991; Correll et al., 1991, 1992; Hoover
et al., 1995, 1996; Storer et al., 1995a,b; Gordon et al., 1996)
suggests that they are highly signi®cant.
The insects involved in this system can be grouped into
genera, as congeneric species perform similar roles in the
ecology of Monterey pine. The interactions among insect
species, and between insects and Monterey pine, can be
generalised as positive, negative, or neutral on each member
of an interacting pair, both in the absence and in the presence of
F. s. pini. The effects of the interactions on the insect genera
may be trophic effects when greater food resources are
provided, and ®tness effects when additional breeding material
becomes available.
The effects of F. s. pini on insect±host treeinteractions
In the absence of F. s. pini, Pityophthorus spp. attack the dead
and dying twigs of Monterey pine, and the occasional branch
tip mortality that they cause does not weaken the tree
signi®cantly (Table 1). The pitch canker fungus has an indirect
effect on this interaction because, by vectoring the pathogen
(Fox & Schultz, 1991; A. J. Storer et al., unpublished) to
healthy branches, twig beetles cause a greatly increased
mortality of Monterey pine branch tips. In a survey of 184
healthy Monterey pine branches without cones, 11.4% died of
pitch canker disease in 1 year, probably as a result of vectoring
by Pityophthorus spp. (Storer et al., 1995a; A. J. Storer et al.,
unpublished). Multiple infections of this type weaken the host
tree as photosynthetic area is lost.
In the absence of F. s. pini, C. radiatae reduces tree ®tness
directly due to its impact on cones and the resulting reduction
in seed crop, but does not threaten the survival of the tree itself
(Table 1). By introducing the fungus to the tree (Hoover et al.,
1996), C. radiatae causes the mortality of branch tips
indirectly, thereby weakening the tree. Ernobius punctulatus
uses tunnels created by cone and twig beetles to infest dying
cones and branches (Table 1). This species can introduce F. s.
pini into cones that are infested by pathogen-free C. radiatae
(Hoover et al., 1996) and hence cause branch tip mortality. In a
survey of 105 healthy cone-bearing branches, 49.5% died from
pitch canker disease in one year, probably as a result of
vectoring by C. radiatae and/or E. punctulatus (Storer et al.,
1995b).
Ips species can cause considerable mortality of Monterey
pines during periods of drought (Ohmart, 1979) and can
produce large populations in cut or fallen host material
(Table 1). The emerging progeny then attack nearby healthy
trees (Furniss & Carolin, 1977). Ips spp. can vector F. s. pini to
Monterey pine (Fox et al., 1991). Fusarium s. pini infections
weaken the tree, and Ips spp. will attack and kill such
weakened trees. In areas where pitch canker disease occurs,
more host material suitable for Ips spp. colonisation is present
(Fox et al., 1990)
As vectors of F. s. pini, all these insect species have an
altered impact on Monterey pine, either from neutral to
negative, or from negative to more strongly negative (Fig. 1).
All these insect species continue to bene®t from Monterey pine
as a food resource, and this bene®t is generally greater in the
presence of F. s. pini, as a result of increased food resources
(Fig. 1).
The effects of F. s. pini on interactions among twig-and cone-infesting insects
In the absence of F. s. pini, C. radiatae does not kill branches,
only cones, and therefore has no effect on Pityophthorus spp.
The feeding activities of Pityophthorus spp. do not have any
bene®t to C. radiatae. Ernobius punctulatus, however, bene®ts
by utilising C. radiatae entrance tunnels to access the cone
(Hoover et al., 1995), and entry tunnels made by Pityophthorus
spp. to enter branches (Fig. 2a). Since E. punctulatus is unable
to infest branch tips or cone whorls not previously infested by
one of the other twig- and cone-feeding species, it has a neutral
effect on C. radiatae and Pityophthorus spp. (Fig. 2a).
The interactions among the genera that infest small branches
(with or without cones) are complex in the presence of F. s. pini,
and depend on which genus of insect has individuals carrying
propagules of the pathogen (Fig. 2b). If Pityophthorus spp.
vector F. s. pini into a healthy branch, the branch ultimately
becomes suitable for infestation by Pityophthorus spp. and by
E. punctulatus, which bene®t from the increased availability of
R
Table 1. Summary of feeding sites and requirements of beetles coevolved with Monterey pine, Pinus radiata.
Beetle species Family Feeding site Requirements
Ips spp. Scolytidae Phloem of larger branches and main stem Generally attacks stressed trees, but is capable of attacking
apparently healthy trees
Pityophthorus spp. Scolytidae Phloem of small branches and twigs Weakened (shade suppressed), and recently broken branches
Conophthorus radiatae Scolytidae Cones and conelets Capable of infesting cones on apparently healthy branches
Ernobius punctulatus Anobiidae Phloem and xylem of large and small
branches, and cones
Requires an entry tunnel made by another insect to enter host.
Feeds on older, drier material than the scolytids
# 1999 Blackwell Science Ltd, Ecological Entomology, 24, 238±243
Modi®cation of coevolved insect±plant interactions 239Modi®cation of coevolved insect±plant interactions 239
entry tunnels made by Pityophthorus spp. (Hoover et al.,
1996). The effect on C. radiatae probably remains neutral,
since there is no evidence that branch tip mortality results in
cone whorls becoming more suitable for infestation by C.
radiatae. If C. radiatae vectors the pathogen to a cone whorl,
branch tip mortality distal to the cone whorl due to pitch
canker disease results in positive effects on Pityophthorus spp.
and E. punctulatus as more suitable feeding and breeding
material becomes available to them.
For E. punctulatus to vector the pathogen to a branch, an
entry tunnel made by C. radiatae or Pityophthorus spp. is
necessary. If one of these species has already introduced the
pathogen into the branch, E. punctulatus carrying inoculum will
have no impact on the ensuing interactions. If C. radiatae
infests a cone, however, but does not vector the pathogen,
E. punctulatus may enter the cone and transmit the pathogen,
and hence have a bene®cial effect on Pityophthorus spp. due to
branch tip mortality distal to the cone whorl (Fig. 2b). Since
L
Fig. 1. Interactions among insects and Monterey pine in the absence or presence of Fusarium subglutinans f. sp. pini.
Fig. 2. Interactions among twig- and cone-infesting insects on Monterey pine (a) in the absence or (b) in the presence of Fusarium subglutinans
f. sp. pini.
# 1999 Blackwell Science Ltd, Ecological Entomology, 24, 238±243
240 Andrew J. Storer, David L. Wood and Thomas R. Gordon240 Andrew J. Storer, David L. Wood and Thomas R. Gordon
Pityophthorus spp. normally infests shaded or dying branches,
the production of entry tunnels for E. punctulatus to vector the
pathogen will not increase the mortality of these branches.
Conophthorus radiatae does not bene®t from the activities of E.
punctulatus in the presence of F. s. pini. Competition between
E. punctulatus and the other cone- and twig-infesting insects is
unlikely, because E. punctulatus feeds on a drier substrate than
C. radiatae or Pityophthorus spp., and this substrate is mostly
available after C. radiatae or Pityophthorus spp. near the
completion of their development (Hoover et al., 1995).
The effects of F. s. pini on interactions among Ipsspp. and twig- and cone-infesting insects
In the absence of F. s. pini, C. radiatae, E. punctulatus and
Pityophthorus spp. do not weaken the host suf®ciently to make
it more suitable for Ips spp. infestation. A tree, tree top or large
branch that is killed by Ips spp., however, provides a resource
for Pityophthorus spp. and E. punctulatus (and possibly C.
radiatae) due to the increased amount of dead and dying small
branches (Fig. 3a). Hence the activity of Ips spp. is bene®cial
to species in at least two genera. Branch tip infection by F. s.
pini resulting from the feeding activities of C. radiatae,
Pityophthorus spp., or E. punctulatus causes a weakening of
the tree and subsequent increased susceptibility to Ips spp.
(Fig. 3b). Trees or branches killed by Ips spp. continue to
provide additional resources (uninfected branches) to
Pityophthorus spp. and E. punctulatus, and possibly more
cone material to C. radiatae. The associations between Ips spp.
and each of these twig-infesting groups are mutually bene®cial
when individual beetles in their populations are carrying the
pitch canker fungus. Individual C. radiatae, or Pityophthorus
spp. that are not carrying the pitch canker pathogen, provide no
bene®t for Ips spp., unless their galleries are occupied by E.
punctulatus carrying F. s. pini. Hence the relationships among
these species could differ according to whether or not
individuals carry the pathogen.
Conclusions
Intrageneric bene®ts of vectoring the pitch canker pathogen
may be evident for Ips spp., Pityophthorus spp. and E.
punctulatus, since vectoring the pathogen may result in
increased amounts of breeding material for congenerics. The
associations between F. s. pini and each insect group are
mutually bene®cial, since the fungus is vectored to a new host,
and the insect species bene®t from a weakened or dead host.
An individual insect carrying the pathogen does not itself
bene®t from introducing the pathogen into the host, as a time
lag is necessary for the pathogen to cause the mortality of the
affected host tissue. Nevertheless, the feeding activities of that
contaminated insect may incidentally bene®t congenerics once
disease development has occurred, whether or not the
congenerics are carrying the pathogen. By associating with
insects, the pitch canker fungus is responsible for killing trees
directly or indirectly, and when this happens, many of its
vectors breed in the recently killed host. A large number of
insect progeny are thus produced, and many of these carry F. s.
pini (Fox et al., 1991; Hoover et al., 1995). A parallel situation
with other insect/vector associations may occur, e.g. Dutch elm
disease, where the vector can multiply as a result of host
mortality caused by the introduction of a pathogenic fungus.
Quanti®cation of the importance of these altered ecological
associations merits further study. Evidence from long-term
R
Fig. 3. Interactions among Ips spp. and twig- and cone-infesting insects on Monterey pine (a) in the absence or (b) in the presence of Fusarium
subglutinans f. sp. pini.
# 1999 Blackwell Science Ltd, Ecological Entomology, 24, 238±243
Modi®cation of coevolved insect±plant interactions 241Modi®cation of coevolved insect±plant interactions 241
studies of disease development suggests that these new
interactions are important components of the ecology of these
insects, as evidenced by the greatly increased branch tip, tree
top and entire tree mortality (Storer et al., 1995b; A. J. Storer
et al., unpublished). Further work is also necessary to
determine the associations among the four twig beetle species
and three engraver beetle species in this system, to clarify
species differences in the interactions described.
Although the association between the pitch canker fungus
and bark beetles is new in California, other associations of
Fusarium spp. with insects are known (e.g. Gillespie &
Menzies, 1993; Sobek & Munkvold, 1995). In addition, all
bark beetle species carry fungi, some of which may be
pathogenic to trees on which the insects feed (Whitney, 1982;
Harrington, 1993). The evolution of these associations may
initially have been rapid, as in the case of the pitch canker
fungus, followed by prolonged coevolution resulting in more
specialised adaptations such as sticky fungal spores and
specialised structures (mycangia) on insects for carrying fungi
(Whitney, 1982; Harrington, 1993). In these situations, it is
hypothesised that the associations between the insect and the
fungus become more obligate as they adapt towards life
together, and away from independent existence.
Changes in the interactions presented here have almost
certainly resulted from the introduction of the pitch canker
pathogen into California. As such, the fungus is an evolu-
tionary novelty (Price et al., 1986) to the coevolved native
Monterey pine/insect/fungal community. It has caused a
disturbance in natural and arti®cial ecosystems, and such
disturbances are important in altering the stability of these
systems (Dinoor & Eshed, 1984). Such a rapid evolution of
associations between organisms may occur naturally as novel
species enter native ecosystems as a result of migration or
other natural dispersal systems.
Acknowledgements
The authors are grateful to P. Bonello, T. D. Bruns, I. Chapela
and D. L. Dahlsten, University of California, Berkeley, for
their reviews of this manuscript. Funding for this work was
provided by the California Department of Forestry and Fire
Protection, and by USDA NRI Competitive Grants 93-37302-
9594 and 96-35302-3821.
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# 1999 Blackwell Science Ltd, Ecological Entomology, 24, 238±243
Modi®cation of coevolved insect±plant interactions 243Modi®cation of coevolved insect±plant interactions 243