6
NEW PERSPECTIVES 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. Modification of coevolved insect–plant interactions by an exotic plant pathogen ANDREW J. STORER, DAVID L. WOOD and THOMAS R. GORDON * 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 significant 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 influence the evolutionary fate of insect, fungus, and tree species simultaneously (Wingfield et al., 1993). Plant pathogens have the potential to alter significantly 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 first identified 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 artificial 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 briefly here. The first 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 intensifies 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, 238–243 Ecological Entomology (1999) 24, 238–243

Modification of coevolved insect–plant interactions by an exotic plant pathogen

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Page 1: Modification of coevolved insect–plant interactions by an exotic plant pathogen

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

Page 2: Modification of coevolved insect–plant interactions by an exotic plant pathogen

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

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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

Page 4: Modification of coevolved insect–plant interactions by an exotic plant pathogen

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

Page 5: Modification of coevolved insect–plant interactions by an exotic plant pathogen

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