Determination of the Ecological and Geographic Distributions of Armillaria Species in Missouri Ozark Forest Ecosystems

Johann N. Bruhn, James J. Wetteroff, Jr., Jeanne D. Mihail, and Susan Burks 1

Abstract.-Armillaria root rot contributes to oak decline in the Ozarks. Three Armillaria species were detected in Ecological Landtypes (ELT's) representing south- to west-facing side slopes (ELT 17), north- to east-facing side slopes (ELT 18), and ridge tops (ELT 11). Armillaria meUea was detected in 91 percent of 180 study plots; was detected with equal frequency in all three ELT's; and was ubiqui­ tous in block 3. Armillaria gaUica was detected in 64 percent of the study plots; was detected least frequently in block 3; and was de­ tected least frequently on ELT 17 in block 3. The distribution of A. tabescens remains incompletely resolved; it is the least abundant species and the most difficult to survey. Armillaria meUea was much more frequently associated with oak mortality than were A. gaUica or A. tabescens, based on isolations from dying or recently killed trees. If these three species compete for substrate, oak decline levels may be influenced by landscape patterns of Armillaria species co-occur­ rence. We hypothesize that oak decline will be most severe in block 3, and especially on ELT 17, where A. meUea most often occurs in the absence of A. gaUica.

Armillaria (Fr.:Fr.) Staude is a white-rot wood (Watling et aZ. 1991). The exact number of decay fungus genus (Fungi, Agaricales) com­ Armillaria species in North America remains prising about 40 species worldwide (Volk and uncertain due to insufficient study. Unfortu­ Burdsall1995, Watling et aZ. 1991). Due to nately, much of the Armillaria literature well similarities in the morphology of Armillaria into the 1980's is of limited value because the mushrooms, mycelial fans, and rhizomorphs, all correct identity of the Armillaria species studied annulate North American Armillaria were widely was never established. This is the initial report thought to belong to a single highly variable of the first formal study of the Armillaria species species (Armillaria meUea) until the late 1970's. influencing forest structure in upland Ozark Following Hintikka's (1973) description of a oak-hickory forests. The three Armillaria spe­ mating test for distinguishing Armillaria species cies encountered were A. gaUica Marxmuller & using pedigreed single-basidiospore isolates, Romagnesi, A. meUea, and A. tabescens (Scop.) great progress has been made in clarifying Emel. biological, ecological and taxonomic issues concerning Armillaria species (Korhonen 1995). A portion of the energy derived by Armillaria The name Armillaria meUea (Vahl:Fr.) Kummer mycelia from wood decay (Garraway et aZ. 1991) now clearly represents a single Armillaria is spent on sexual reproduction of airborne species, the type species of the entire genus basidiospores on mushroom gills. Each spore that successfully germinates to colonize a suitable woody substrate (food base) generally mates with another sexually compatible 1 Research Associate Professor, Senior Research germling to form a genetically unique individual Technician, and Associate Professor, respec­ ("genet," sensuHarper 1977) thatmaybecome tively, Department of Plant Pathology, 108 established in the landscape as an agent of Waters Hall, University of Missouri, Columbia, wood decomposition and perhaps of root dis­ MO 65211; and Forest Pathologist, Missouri ease and forest decline (Anderson and Kohn Department of Conservation, P.O. Box 180, 1996, Guillaumin et aZ. 1991). Jefferson City, MO 65102. 257 ------

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Genets of all ArmiUaria species are functionally Land Type (EL11 characteristics (Bruhn et aL territorial, enlarging through sequential coloni­ 1994, Korhonen 1978, Rishbeth 1982). The zation of woody food bases by branching, cord­ mechanisms by which neighboring ArmiUaria like rhizomorph systems and/ or growth across genets of the same or different species interact root contacts and grafts (Gregory et al. 1991, to allocate space among themselves are not yet Morrison et al. 1991, Redfern and Filip 1991). clear. Where the perimeters of Armillaria genets Rhizomorph growth is fueled with energy and meet or overlap, genets may interact as a result nutrients derived from food base decay (Ander­ of niche overlap and competitive exclusion son and Ullrich 1982, Garrett 1956, Rishbeth (Leibold 1995, Mohammed and Guillaumin 1972) and from the soil through which the 1989). Genets of different Armillaria species rhizomorphs grow (Morrison 1975). Armillaria may circumvent each other as a result of differ­ rhizomorph production is generally increased ent colonization strategies (Legrand et al. 1996). when using hardwood compared with conifer Nevertheless, the activity levels of Armillaria food bases (Redfern and Filip 1991). Because genets adjust to changes in the environment Armillaria species do not produce asexual (e.g., climate, defoliation, vegetation manage­ spores, Armillaria genets are potentially con­ ment) that affect the supply of food bases and tinuous in the forest floor. Armillaria genets are the vulnerability of potential hosts (Bruhn et al. also potentially long-lived and can achieve great 1994, Lonsdale and Gibbs 1996, Wargo 1996, size (Anderson and Kohn 1996, Bruhn et aL Wargo and Harrington 1991). The spatial 1997, Korhonen 1978, Legrand et aL 1996, arrangements and ecological attributes of Rishbeth 1991, Shaw and Roth 1976, Smith et Armillaria genets help shape long-term forest aL 1992), especially when compared with most community structure in response to perturba­ vegetation. tions (Lundquist 1993, Worrall and Harrington 1988), because each extant combination of ArmiUaria species differ in host preference and genets contributes differently to the regulation virulence; genets of the same species can also of stand structure and composition. differ in virulence. Studies elsewhere of Armillaria species that also occur in the Ozarks Armillaria species are often implicated as oppor­ have concluded that A. meUea is much more tunistic root parasites contributing to forest virulent than either A. gaUica or A. tabescens declines incited by various stress events (Bauce (Gregory et al. 1991, Guillaumin et aL 1993, and Allen 1992, Clinton et al. 1993, Houston Redfern and Filip 1991, Rishbeth 1991). 1992, Johnson and Law 1989, Kile et aL 1991, Armillaria meUea and A. gaUica are generally Wargo 1996). Both excess moisture and considered to be much more common than A. drought during the growing season are capable tabescens (which can be locally abundant). of inciting Armillaria root disease (e.g., Lonsdale Armillaria meUea is capable of attacking and and Gibbs 1996, Wargo and Harrington 1991). killing a wide variety of hardwoods and a Rhoads (1956) found that droughty acidic sites smaller range of conifers (mainly non-resinous predisposed trees to attack in Florida, whereas species). Armillaria gaUica is more restricted to poorly drained soils on former oak sites predis­ colonizing dying or dead material and causing posed grape plants to attack in Missouri butt rot of hardwoods. In western Europe, A. (Rhoads 1925). A study of oak decline in up­ tabescens is considered the least virulent of the land Ozark forests showed that the growth rates three species, largely restricted to hardwood of trees that eventually died did not recover stumps. A notable exception is primary parasit­ following severe drought (compared to similar ism by A. tabescens of exotic Eucalyptus species trees that remained healthy), and that growth of in southwest France. North American A. declining trees was further depressed with each tabescens has a large host range and may be succeeding drought (Dwyer et aL 1995). This somewhat more virulent than European A. scenario is consistent with a combined tabescens (Sinclair et al. 1987). However, Armillaria+ drought etiology. A relationship Rhoads (1925, 1956) indicated that exotic and has been recognized between predisposing cultivated tree species were much more suscep­ stress events (e.g., drought, late frost, defolia­ tible than native tree species to North American tion), Armillaria root disease, and oak decline A. tabescens, especially when planted on land and mortality in the Missouri Ozarks (Johnson previously cleared of oak forest. and Law 1989, Law and Gott 1987), though the identities of the ArmiUaria species involved and ArmiUaria species (and genet) distributions are the nature and extent of their involvement and related to long-term vegetation and Ecological interactions were not determined. The black/ 258

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Table I.-Distribution of Armillaria study plots among statistical blocks,forest sites, silvicultural systems, ecological/and types, and type of harvest activity

Silvie. Harvest Total Harvested Block Site system1 treatment 1 ELT2 plots3 plots3

1 NHM 11 6 0 17 6 0 18 7 0 2 UAM s 11 7 7 s 17 6 3 s 18 8 5 3 EAM I 11 6 2 I 17 8 1 c 17 8 1 I 18 6 4 c 18 6 1 2 4 UAM s 11 6 6 s 17 7 5 s 18 6 6 5 EAM I 11 7 4 c 17 8 1 I 18 8 1 c 18 8 3 6 NHM 11 6 0 17 6 0 18 7 0 3 7 UAM s 11 7 5 s 17 8 4 s 18 6 2 8 NHM 11 6 0 17 6 0 18 6 0 9 EAM c 11 6 1 17 6 0 c 18 8 2

1 Silvicultural system: NHM indicates no-harvest management(-); UAM indi- cates uneven-aged management by single-tree and group selection (S); EAM indicates even-aged management by clearcutting (C) and thinning (I). None of the six ELT 17 Armillaria study plots in site 9 received harvest treatment in 1996. 2 Ecologica1landtype, based on slope and aspect: ridges (ELT 11), south- and west- facing side slopes (ELT 17), and north- and east-facing side slopes (ELT 18). 3 Total plots are the number of plots examined for Armillaria in the site. Harvested plots are the number of plots examined for Armillaria harvested by the indicated treatment.

260 were abundant enough for us to detect its base of trees was collected preferentially. Dur­ presence. Thus, our experimental hypothesis ing every visit, any imminent or recent tree was: mortality was noted and evaluated for presence of mycelial fans, and these were always col­ H : Each Armillaria species occurs with equal lected. Living trees with abnormally few live 0 frequency irrespective of MOFEP block, ELT, leaves (and many of these abnormally small and or proposed silvicultural treatment. chlorotic) were categorized as "dying." Dead trees retaining fine twig structure and any dead This hypothesis was evaluated separately for A. leaves were categorized as "recent-dead" (table gallica and A. meUea using the GLM algorithms 2). During at least one visit, all woody debris, of the SAS statistical package to perform analy­ stumps, and dead trees were carefully examined sis of variance (ANOVA). MOFEP block, ELT, for presence of rhizomorphs. Several and silvicultural treatment served as classifica­ rhizomorph samples were collected from each tion variables. The response variable was the plot whenever possible. Evaluation of a plot transformed proportion of plots within a site in was considered complete only after it had been which the Armillaria species of interest was searched thoroughly for all these forms of found. The transformation used was the arcsin evidence. The locations of all field collections of the square root of the calculated proportion were mapped for use in ensuing studies of the (Steel and Torrie 1980). Because of the small spatial relationships between Armillaria popula­ number of plots per site, the response variable tions, tree vegetation, and oak decline. was weighted by the inverse of its variance: 1 [p( 1-p)/n]- • The treatment*block interaction Field estimation of an Armillaria genet's patho­ was used as "error a," to evaluate the signifi­ genicity requires careful consideration of avail­ cance of differences among treatments and able evidence, including (1) the condition of the blocks. The treatment*ELT*block interaction woody substrates from which isolates are was used as "error b," to evaluate significance of taken, and (2) the source tissues of the isolate differences among ELT's and the treatment*ELT (Gregory et aL 1991, Morrison et aL 1991). The interaction. Occurrence data for A. tabescens presence of an Armillaria mycelial fan in the will be analyzed after additional field isolates root collar cambial region of a dying or recently are collected and identified. killed tree constitutes strong evidence of patho­ genicity, because mycelial fans represent lethal Because the ANOVA above combines the 5 to 8 colonization of the invaded root cambium binomial presence/absence data for each ELT/ tissue. Mycelial fans under the bark of long­ site combination into a single proportion, its dead trees may represent necrotrophic coloniza­ ability to detect ELT differences is severely tion unrelated to pathogenicity. Although limited. Because of the pre-harvest timing of rhizomorphs are the organs of root infection, this evaluation, the silvicultural treatments can rhizomorphs alone are not strong evidence of be set aside to examine the distributions of A. pathogenicity. Rhizomorphs on root surfaces gallica and A. meUea among ELT's in each of the are either non-pathogenic or have not had three blocks of sites using contingency table appropriate opportunity (e.g., through host analysis of the raw data. We used the general stress) to demonstrate their pathogenicity. association statistic (GA) of the Cochran-Man­ Because Armillaria species fruit well on the tel-Haenszel test (Agresti 1990) for this purpose. forest floor and on woody debris in proximity to living trees, fruiting near a tree is not strong Sampling evidence of pathogenicity. Based on these considerations, all of the above structures were Each entire 0.2-ha plot was thoroughly used to determine the presence/absence within searched at least once, depending on what was plots of each Armillaria species, but only the collected and what could be observed. The presence of a mycelial fan in the root collar of a forest floor was scanned carefully for fruiting of dying or recently killed tree was interpreted as A. mellea and A. tabescens during at least one strong evidence of pathogenicity. visit when each species was known to be fruit­ ing on the site. When fruiting was found on a Sample Analysis plot, at least one collection was made represent­ ing each mushroom morphology type (based on Armillaria field isolates representing each study color and stature) encountered. Fruiting at the plot were derived from (1) mycelial fans on dying

261 ~ • IYJ(Q)JFJEIP------

1 Table 2.---Sources of MOFEP Armillaria study isolates •

Armillaria species Armillaria species Substrate Source gallica mellea Substrate Source gallica mellea

Healthy Debris or Dead ;:::2 yrs red oaks (subgenus Erythrobalanus) red oaks mycelial fan or wood 0 0 mycelial fan or wood 3 39 mushroom 0 8 mushroom 0 68 rhizomorph 0 0 rhizomorph 29 2 white oaks (subgenus Leucobalanus) white oaks mycelial fan or wood 0 0 mycelial fan or wood 1 4 mushroom 0 2 mushroom 0 20 rhizomorph 0 0 rhizomorph 13 0 hickories (Carya species) hickories mycelial fan or wood 0 0 mycelial fan or wood 1 0 mushroom 0 mushroom 0 2 rhizomorph 0 0 rhizomorph 21 0 other hardwoods2 other hardwoods2 mycelial fan or wood 0 0 mycelial fan or wood 3 3 mushroom 0 1 mushroom 0 22 rhizomorph 2 0 rhizomorph 59 0 pine (Pinus echinata) pine mycelial fan or wood 0 0 mycelial fan or wood 1 0 mushroom 0 0 mushroom 0 0 rhizomorph 0 0 rhizomorph 0 Total (healthy) 2 12 Total (debris or dead;::: 2 yrs) 132 160

Dying or Recent-dead Total (all 3 categories) 145 252 red oaks mycelial fan or wood 3 32 mushroom 0 41 rhizomorph 5 1 white oaks mycelial fan or wood 2 mushroom 0 2 rhizomorph 0 0 hickories mycelial fan or wood 0 0 mushroom 0 0 rhizomorph 0 0 other hardwoods2 mycelial fan or wood 0 0 mushroom 0 0 rhizomorph 0 0 pine mycelial fan or wood 1 0 mushroom 0 0 rhizomorph 0 3 Total (dying or recent-dead) 11 80

1 The 89 isolates not represented include: A. gallica- 15 rhizomorph isolates from unidentifiable woody debris, 1 isolate from a bait potato, and 1 fan isolate with incomplete data; A. me/lea - 39 forest floor :nushroom isolates, 1 fan isolate with incomplete data, and I isolate from unidentifiable woody debris; A. tabescens - all 31 isolates. 2 Other hardwoods includes dogwood, red maple, unidentifiable oak, sassafras, and black walnut.

262

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All All

region region

conducted conducted

pairing pairing

genetic genetic

we we

agar agar

fruit fruit

tests tests

speciation. speciation.

Conversion Conversion

or or

on on

on on

span span

much much

meUea meUea

genets genets

analysis analysis

preponderance preponderance

genets genets

isolate isolate

of of

two two

basis basis

diploid diploid

unidentified unidentified

required required

their their

of of

(Darmono (Darmono

we we

genets genets

Collection Collection

a a

nearly nearly

and and

Shaw Shaw

Armillaria Armillaria

other other

evaluated evaluated

to to

mating mating

isolate isolate

A. A.

species species

large large

(IGS) (IGS)

acid acid

to to

rely rely

of of

of of

dark. dark.

1993-1995 1993-1995

the the

the the

40 40

of of

of of

isolates isolates

33·c. 33·c.

speciate speciate

PCR PCR

RESULTS RESULTS

These These

we we

between between

enzyme enzyme

some some

tabescens tabescens

our our

with with

readily readily

this, this,

these these

the the

in in

(e.g., (e.g.,

for for

Rizzo Rizzo

on on

(Harrington (Harrington

at at

to to

or or

the the

morphology morphology

potentially potentially

each each

complete. complete.

diploid). diploid).

of of

A. A.

laborious, laborious,

1991). 1991).

isolates isolates

for for

detected detected

of of

analysis analysis

do do

1994 1994

isolates isolates

basis basis

Sample Sample

not not

tannic tannic

enough enough

spacer spacer

in in

isolate isolate

methods methods

of of

types types

Armi.Uaria Armi.Uaria tests tests

incubation incubation

of of

paired paired

the the

genets genets

plots. plots.

al.. al..

1992). 1992).

To To

Armillaria Armillaria

paired paired

dark dark

do do

the the

and and

on on

the the

distinguish distinguish

currently currently

1978, 1978,

included included

late late

field field

for for genets

PCR PCR

field field

et et

60 60

operon operon

nearly nearly

operon operon

"diploid-haploid" "diploid-haploid"

al.. al..

of of

the the

large large

culture culture

24·c 24·c

both both

to to

for for

obtained obtained

on on

pairings pairings

in in required required

isolates isolates

are are

the the

tester tester

of of

derived derived

developed developed

We We

is is

if if

genets genets

weeks weeks

that that

et et

genets genets

plot. plot.

and and

at at

and and

efficient efficient

in in

(presumed (presumed

7 7

any any

7 7

be be

and and

RNA RNA

RNA RNA

are are

all all

intergenic intergenic

plots, plots,

distinguished distinguished

study study

isolates isolates

1995). 1995).

Establishment Establishment 36 36

compatibility compatibility

Armillaria Armillaria

plots, plots,

study study

neighboring neighboring

and and

Considering Considering

ing ing

1938) 1938)

territory territory

that that

mal mal

haploid haploid

Smith Smith

mal mal

Armillaria Armillaria systems systems

the the

RFLP RFLP

polyphenoloxidase polyphenoloxidase

possible possible Having Having

isolates isolates

technique technique

(Korhonen (Korhonen

leamed leamed

consuming consuming

MEA MEA

incubation incubation

after after

more more MOFEP MOFEP

so-called so-called

Garraway Garraway

be be rate rate

occurs occurs

tion tion

Because Because

haploid haploid

lates lates

isolates isolates

genets genets

may may

fruiting fruiting

for for

at at

bark bark

2-

B. B.

by by

with with

or or

by by

malt malt

to to

to to

were were

repre­

of of

and and

identity identity

con­

Prod­

pre­

from from

floor, floor,

con­

are are

intemal intemal

were were

200 200

with with

lengths lengths

Field Field

genet genet

sulfate. sulfate.

condi­

of of

Center Center

/v) /v)

this this

labora­

distilled distilled

for for

isolates isolates

1996). 1996).

minutes, minutes,

made made

Bacterial Bacterial

tester tester

van van

voucher voucher

samples samples

isolates isolates

cultures cultures

Depart­

genet genet

James James

(w (w

dying dying

7 7

and and

solidified solidified

the the

were were

root root

surface surface

tests tests

species species

towel, towel,

with with

al.. al..

taken taken

characteristic characteristic

forest forest

For For

mushroom mushroom

species species

genet genet

or or

Forest Forest

The The

dishes dishes

to to

applied applied

own own

isolates isolates

species species

the the

window window

single-basid­

traditional traditional

Dr. Dr.

a a

for for

containing containing

et et

were were

isolates isolates

to to

field field

tester tester

diploid diploid

sterile sterile

necessary necessary

a a

and and

using using

from from

the the

as as

(1.05-percent (1.05-percent

was was

agar agar

a a

by by

bark bark

fan fan

our our

field field

of of

and/ and/

especially especially

in in

Botany Botany

petri petri

paper paper

The The

tests tests

University University

single-basidiospore single-basidiospore

with with

Working Working

USDA USDA

on on

known known

Isolates Isolates

rhiZomorph rhiZomorph

from from

to to

WI, WI,

1991). 1991).

sections. sections.

radially, radially,

medium medium

was was

1989). 1989).

as as

us us

from from

to to

3-percent 3-percent

the the

repositories repositories

set set

streptomycin streptomycin

colonized colonized

dishes dishes

bleach bleach

on on

matings, matings,

It It

and and

of of

to to

occur occur

identified identified

a a

al.. al..

water water

of of

on on

Armillaria Armillaria

blea.ch blea.ch

clean clean

torn torn

isolations isolations

well well

identified identified

removing removing

et et

which which

agar. agar.

storage storage

1969). 1969).

5+-cm 5+-cm

isolation isolation

Mycelial Mycelial

a a

debris debris

cultures cultures

History, History,

culture culture

petri petri

means. means.

eliminated eliminated

Botany, Botany,

(Guillaumin (Guillaumin

tissue tissue

incompatibility incompatibility

Bruhn Bruhn

extract extract

first first

as as

Rhizomorph Rhizomorph

in in

based based

used used

isolates isolates

in in

(w/v) (w/v)

obtained obtained

/v) /v)

rhizomorphs rhizomorphs

for for

in in

Madison, Madison,

of of

Research, Research,

converted converted

single-basidiospore single-basidiospore

species species

unidentified unidentified

were were

then then

milliliter milliliter

isolates isolates

IL, IL,

dishes dishes

term term

sterilizing sterilizing

Initial Initial

1-mm-long 1-mm-long

(w (w

was was

dish dish

changes changes

and and

are are

provided provided

gills. gills.

(2) (2)

[fuite [fuite

household household

dry dry

permanent permanent

sections sections

malt malt

fan. fan.

were were

an an

woody woody

compatible compatible

tests tests

have have

(MEA) (MEA)

fungal fungal

per per

soaking soaking

several several

by by

carefully carefully

Natural Natural

was was

specimens. specimens.

household household

caps caps

as as

or or

the the

mushrooms. mushrooms.

tissue tissue

In In

(Dept. (Dept.

/v) /v)

long-

petri petri

and and

determining determining

the the

from from

of of

petri petri

Armillaria Armillaria

isolates isolates

we we

of of

by by

cells cells

vegetative vegetative

reliable reliable

(Guillaumin (Guillaumin

(w (w

them them

"tester" "tester"

trees, trees,

using using

agar agar

and and

(3) (3)

Armillaria Armillaria

in in

2-percent 2-percent

of of

becomes becomes

in in for for

Mycology Mycology

Although Although

Chicago, Chicago,

bark, bark,

(Richter (Richter

genet genet

isolates isolates

one one

mating mating

seiVe seiVe

maintained maintained

trees trees

cultures. cultures.

2-percent 2-percent

Laboratory, Laboratory,

or or

above above

trama trama

20-percent 20-percent

dead dead

by by

expose expose

(haploid) (haploid)

tion. tion.

morphological morphological

isolate isolate

purpose, purpose,

identified identified

representing representing

means means

is is

Each Each least least

mated mated

identity identity extract extract

ducted ducted

iospore iospore

Toronto). Toronto).

sentative sentative

through through

Field Field

mushroom mushroom

tory, tory,

ment, ment,

Anderson Anderson

seiVed seiVed

ucts ucts

Museum Museum

Forest Forest

percent percent

20-percent 20-percent

contamination contamination

culturing culturing

obtained obtained

derived derived

NaOCl) NaOCl)

water water

to to

in in

were were

blotting blotting

intact intact

cap cap

with with

identifications identifications

Tieghem Tieghem

culture culture

micrograms micrograms Mushroom Mushroom

pure pure

taining taining and/ and/ dead dead

transferring transferring or or

because because just just ~M@W~W------"""

permanent MOFEP plots have been identified as 7, 1994, but poorly in mid-October 1995. Final representing 431 genets belonging to three evaluation of A. tabescens distribution is post­ Armillaria species (140 genets of A. gaUica, 261 poned pending collection of additional field data genets of A. meUea, and 30 genets of A. during a year favorable for fruiting. tabescens). No genet was encountered on more than one of our study plots. As many as four Isolates of A. gaUica, A. meUea, and A. genets and three species have been recovered tabescens, respectively, were derived from myce­ from individual plots. lial fans at the root crowns of 5, 33, and 3 declin­ ing or recently killed hardwood trees (table 2, A. Armillaria gallica was collected mostly as tabescens data not shown). This represents 4 rhizomorphs (90 percent of collections). seldom percent, 13 percent, and 10 percent, respectively, as mycelial fans (9 percent); we have not yet of the isolates included in table 2 (A. tabescens found A. gaUica fruiting in the study plots. data not shown). Armillaria meUea appears to be Armillaria meUea has been collected rarely as quite virulent, A. tabescens appears to be inter­ rhizomorphs (2 percent), and mostly as mycelial mediate in virulence, and A. gallica appears to be fans (27 percent) or mushrooms (70 percent); A. relatively avirulent (though probably capable of mellea fruited well October 11-22, 1993, August butt rot). 24 to September 13, 1994, and October 3-11, 1995. Armillaria tabescens has never been Armillaria Species Distributions collected as rhizomorphs, but mostly as myce­ lial fans (52 percent) or mushrooms (48 per­ Results of our 3-year survey clearly portray the cent); A. tabescens fruited well mid-August to pre-treatment distributions of A. gaUica and A. September 8, 1993 and August 26 to September mellea in MOFEP's upland forests (table 3).

Table 3.-Frequencies of detection of Armillaria gallica and A. mellea on 180 randomly selected 0.2-ha permanent 1 vegetation plots, by ELT within the nine MOFEP sites •

Species ELT2 Status 1 2 3 4 5 6 7 8 9 Total

A. gallica 11 Present 6 6 3 4 7 5 3 3 3 40 Absent 0 1 3 2 0 1 4 3 2 16

17 Present 3 3 5 4 5 5 1 0 2 28 Absent 3 3 3 3 3 7 6 4 33

18 Present 6 8 5 6 6 5 4 2 4 46 Absent 1 0 1 0 2 1 2 4 3 14

A. mellea 11 Present 4 7 5 6 4 5 7 6 6 50 Absent 2 0 1 0 2 1 0 0 0 6

17 Present 6 5 7 6 6 5 8 5 6 54 Absent 0 1 2 1 0 1 0 7

18 Present 7 6 4 6 8 7 6 6 8 58 Absent 0 2 1 0 0 0 0 0 0 3

1 Tabular values are the numbers of plots for which evaluation is complete in which the specified Armillaria species has been detected (present) or has not been detected (absent). 2 Ecological land type, based on slope and aspect: ridges (ELT 11), south- and west-facing side slopes (ELT 17), and north- and east-facing side slopes (ELT 18). 3 Sites 1-3 comprise statistical block 1; sites 4-6 comprise statistical block 2; sites 7-9 comprise statistical block 3. Sites 1, 6, and 8 will remain uncut; sites 2, 4, and 7 are receiving uneven-aged management; sites 3, 5, and 9 are receiving even-aged management. 264

P P

265 265

3: 3:

and and

2, 2,

= =

only only

study study

= =

plots. plots.

three three

per­

on on

de­

GA GA

slope slope

A. A.

2.551, 2.551,

df df

slope slope

plots, plots,

block block

90 90

0.849; 0.849;

15 15

with with

plots, plots,

the the

= =

= =

1: 1:

three three

slope slope

were were

test test

and and

P P

side side

absence absence

side side

and and

on on

GA GA

I I

slope slope

only only

2, 2,

the the

7.138, 7.138,

0.120; 0.120;

frequencies frequencies

west­

5 5

side side

Significant Significant

occurred occurred

= =

contingency contingency

among among

2: 2:

chance. chance.

= =

= =

(block (block

on on

ELT's ELT's

on on

ridgetop ridgetop

side side

>F

P P

plots, plots,

gallica gallica

and and

df df

3 3

the the

facing facing

no-harvest no-harvest

GA GA

of of

frequencies frequencies

0.947 0.947

0.844 0.844

0.588 0.588

0.046 0.046

2, 2,

0.222 0.222

0.839 0.839

0.423 0.423

0.036 0.036

Pr Pr

A. A.

detected detected

in in

or or

mellea mellea

presence presence

using using

block block

= =

random random

gallica gallica

and and

study study

3: 3:

ofvariation. ofvariation.

of of

east-

west-facing west-facing

0.377). 0.377).

south-

the the

A. A.

1 1

df df

by by

0.327, 0.327,

= =

A. A.

was was

occurred occurred

to to

to to

detected detected

raw raw

east-facing east-facing

in in

1.1 1.1

1.7 1.7

0.2 0.2

0.2 0.2

0.6 0.6

ridgetop ridgetop

8.5 8.5

7.4 7.4

0.2 0.2

F4 F4

= =

P P

1, 1,

and and

block block

percent percent

three three

0.030; 0.030;

block block

to to

of of

sources sources

west-facing west-facing

2, 2,

ridges, ridges,

the the

detected detected

was was

GA GA

= =

50 50

= =

blocks blocks

4.248, 4.248,

to to

the the

of of

gallica gallica

P P

management, management,

3 3

gallica gallica

north-

south-

each each

gallica gallica

6.1 6.1

1: 1:

5.0 5.0

= =

0.7 0.7

9.3 9.3

block block

df df

in in

magnitude magnitude

19.1 19.1

13.6 13.6

38.8 38.8

20.0 20.0

73.5 73.5

24.5 24.5

39.3 39.3

SS

2, 2,

A. A.

of of

were were

of of

A. A.

664.5 664.5

0.279; 0.279;

north-

with with

aspect: aspect:

In In

for for

distributions distributions

difference difference

Typem Typem

= =

Cochran-Mantel-Haenszel Cochran-Mantel-Haenszel

percent percent

meUea meUea

indicated indicated

GA GA

= =

3, 3,

of of

south-

df df

P P

among among

and and

no no

A. A.

variation. variation.

the the

79 79

ELT's ELT's

greater greater

(block (block

the the

2: 2:

1.950, 1.950,

the the

analysis analysis

of of

which which

2, 2,

of of

4 4

2 2 4 4

2 2

2 2

df2 df2

Armillaria Armillaria

4 4

2 2

2 2

4 4

2 2

of of

= =

12 12

12 12

percent percent

percent percent

uneven-aged uneven-aged

ELT. ELT.

block block

= =

with with

of of

slope slope

0.028). 0.028).

slopes. slopes.

53 53

plots. plots.

compared compared

cent cent

55 55

percent percent = =

mellea mellea

6.989, 6.989,

In In study study

data, data, df df

plots, plots,

differences differences

GA GA

tected tected

table table

examined examined

ELT's ELT's

with with

block block

which which

When When

on on

and and

source source

side side

F-statistic F-statistic

= =

18 18

2. 2.

98 98

3, 3,

3, 3,

in in

based based

was was

associated associated

an an

(P (P

7-9, 7-9,

it it

distribution distribution

management, management,

treatment, treatment,

and and

indicated indicated

than than

de­

and and

and and

and and

and and

3), 3),

1 1

common common

8). 8).

east-facing east-facing

3 3

same same

blocks blocks

2, 2,

2, 2,

values values

sites sites

the the

treatments treatments

gallica gallica

A. A.

meUea meUea

was was

1, 1,

1, 1,

and and

observing observing

the the

and and

was was

A. A.

no-harvest no-harvest

(table (table

with with

A. A.

evaluating evaluating

for for

even-aged even-aged

differences differences

86, 86, 88,

(i.e., (i.e.,

39, 39, 39,

block block

of of

respectively respectively

of of

6, 6,

1 1

blocks blocks

squares squares

3 3

(Treatment*ELT*Block) (Treatment*ELT*Block)

silvicultural silvicultural

of of

(Treatment*ELT*Block) (Treatment*ELT*Block)

(Treatment*Block) (Treatment*Block)

in in

(Treatment*Block) (Treatment*Block)

in in

for for

in in

the the

no no

north-

3, 3,

1, 1,

among among

gallica gallica

and and

of of

a a

b b

a a

b b

sites sites

blocks blocks

blocks blocks

ecologicallandtype ecologicallandtype

statistical statistical

or or

meUea meUea

distributional distributional

for for

with with

record record

table table

freedom. freedom.

in in

in in

and and

block, block,

block block

A. A.

associated associated

contrast, contrast,

sums sums

Error Error

ELT ELT Treatment*ELT Treatment*ELT

Treatment Treatment

percent percent

Error Error

Error Error

Treatment Treatment

Block Block

Error Error

ELT ELT Treatment*ELT Treatment*ELT

Source Source

Block Block

variation

treatment: treatment:

found found

ELT, ELT,

of of

(sites (sites

2 2

nine nine

probability probability

to to

in in

three three

0.036) 0.036)

In In

slopes, slopes,

detected detected

detected detected

1, 1,

detected detected

39 39

SS: SS:

all all

= =

plots plots

plots plots

the the

was was

Armillaria Armillaria

the the

variance variance

5). 5).

III III

occurrence occurrence

side side

(P (P

in in

F: F:

complete complete

degrees degrees

was was

and and

significant significant

Though Though

relative relative

compared compared

of of

F-statistic F-statistic

> >

2. 2.

mellea mellea

gallica gallica

study study

study study

distribution distribution

blocks blocks

df: df:

Pr Pr

F: F:

Silvicultural Silvicultural

Type Type

treatment treatment

ANOVA ANOVA

78, 78,

4). 4).

only only

5 5

4 4

1 1

2 2

3 3

facing facing

management; management;

Species Species

A. A.

A. A.

(table (table

plots plots

ELT's ELT's

in in

and and

among among

ubiquitous ubiquitous

gallica gallica

commonly commonly

the the

the the

is is

species species

meUea meUea

The The

1 1

tabescens tabescens

75, 75,

Ranch) Ranch)

A. A.

of of

of of

detected detected

(table (table

in in

A. A.

less less

5). 5).

plots plots

three three

4.-Analysis 4.-Analysis

MOFEP MOFEP

nearly nearly

Peck Peck

both both

all all

ELT's. ELT's.

blocks blocks

Table Table

tabescens tabescens

(table (table

or or

study study

on on

percent percent 0.046) 0.046)

respectively. respectively.

differences differences

management management

Armillaria Armillaria

tected tected

much much

percent percent

respectively respectively

for for

in in

the the

where where

was was

Armillaria Armillaria ANOVA ANOVA ~M@W~W------­

very This

As

Because We

Armillaria A. the that Rhoads floor, tion A. has previously abundant to conditions that should provide two than nine produced regularly tions. provide each trees, of did suming

strict occurrence collected tabescens

permanent north- (1)

1

Species Table

266

Ecologicallandtype,

gallica

mellea

A.

environmental

the

produces

have

not

"pre-treatment"

will

proven

with

were

an

slow

represents

gaUica

MOFEP

5.-Distribution

A.

species.

to

(2)

sense)

but

study

involve

east-facing

fruit

effective

mycelial mycelial

meUea, that

(1925).

still

causes

Armillaria

confirmed

as

logging

in

process

collected.

the

was

of

over species

reported

for

Absent

Absent

Present

Present

Status

vegetation

more

of

mid

or

mycelial

reflect

and

in

genets

the

few

progressed,

sites

vast

A.

Although

fruiting,

rarely A.

a

the

the

and

the

The

little

to

survey

three

gaUica

fans,

fans

different

or

was

side

damage

difficult

DISCUSSION

meUea,

change),

(in

based

on

over

majority

of

next

late

Ozarks;

genet

pre-operational

the no

detected

from

first

distribution

(4)

Armillaria

distribution

slopes

fans

Armillaria

collected

contrast

mortality

a

rarely

on

11

15

6 18 16

study

(3)

species.

rhizomorphs

we

4

3

stratified

appears

the

presence

on

autumn,

and

for

year

A.

demonstration

recently

because

southem

it

establishment

fruits

documentation.

to

from search

slope

expect

(ELT we

gallica

period

all

became

A.

of

Block

virulent

A.

finalize

plots

in

or

17

11

feel

the

gallica to

three

tabescens

2 9

2

as

and

that mellea

meUea

recently

18).

less

the

Depending

two,

to

record

was

genet

sample

of

of

1

strategy

to rhizomorphs.

killed

rhizomorphs

A.

apparently

safe

located

1993-1995.

aspect:

be

Missouri

next

three distribu­

A.

apparent would

in than

complete

predictably

and

species

in

enough

tabescens

18

19

17

commonly

the

3

(in

fruited

tabescens

in

the

response

conjunc­

for

trees,

A.

of

killed

is

year

ridges

was

of

the

as­

least

those

for

in

mellea

the

forest

a

fl.

on the

by

all

to

or

it

(ELT

11

6 14 16

15

3

3

among

window

was

Armillaria with late

moisture necessarily the Both 11), species tionally fans, record. tember apparently for searching ations, Fruiting

late-October, ing taken ing delayed uted mycelial ences these mycelial advent timing equate

species, cause of and detected

detected

tabescens.

Block2

all

17

17

-~---~------

the

them

4

7

south-

was

provided

autumn

summer

A.

quite

which

of

A.

and plots

three

in

three

the

it

and

tabescens we

moisture.

of

the

was

1995

well

meUea

not of

and

Dry

which

appears

of

fan, fans

their

in

species,

to

differently.

in

cold

21

18

17

mushrooms

longest

unpredictable

for

mellea

time,

placed

study

3

0

examined.

A.

west-facing

depending

three abundance

they

64

overlap.

In

species

mid

occurring.

restricted

with

weather

in

greatly

the

if

was

and

and

fruiting

and

meUea

biologies

general,

autumn

percent

was

moisture

and

1993,

ELTs

and

produce to

majority

to

species,

A.

was

although

was

decay highest

apparently

focused

time

Armillaria

never

11

late

19

A.

in be recovered

1

9

0

diminished

9

meUea,

,

these

was

Based

in

side

in

one

from

the

the

the

mainly

tabescens

to

Armillaria underscore

the

to

of

annual

nights

of

The

summer. and

each

late

collections

as

Block3

is

from

a

slopes

rhizomorphs,

associated

the

survey,

A.

of

of

detected

most

survey

least

relative

on

least

7 18 17

17

19

windows

single

abundant,

mid-August

the

rhizomorphs.

3

1

on

or

block.

the

August

differences

records

the

tabescens

tabescens

responsible

plots

rhizomorph,

on

infrequently

year

as

hardly

(ELT

these

fruiting

survey

widely

frequently

need

common.

fruiting

wettest

fruited

abundant

well

gallica

priority

2-

in

It

20

10

abundance

major

9

in 0 examined,

to

when

17),

can

and

part

did

to

for

with

consider­

to

year,

91

as

at

later

of

distrib­

3-week

fruiting of

has

and

mycelial

through

among

this

years

not

search

by

fruit

was

excep­

all.

Sep­

ad­

percent

its

be­

differ­

on

fruit­ for

each

the

The

Fruit­

as

A.

in

in

on

A. A.

A. A.

by by

267 267

is is

and and

genet genet

niche niche

that that

all all

genets genets

A. A.

sug­

pat­

al. al.

in in

are are

se­

certain certain

less less

tempo­

of of

when when

al. al.

vs. vs.

compo­

oak oak

of of

the the

the the

by by

greater greater

gaUica. gaUica.

et et

disease disease

occur occur

differ­

compet­

that that

for for

gallica, gallica,

The The

to to

in in

Ulti­

of of

mitigate mitigate

selected selected

et et

Harrington Harrington

of of

boundary, boundary,

to to

A. A.

anticipated. anticipated.

of of

objectives objectives

to to

gaUica gaUica

its its

MOFEP MOFEP

A. A.

structure structure

found found

landscape landscape

have have

meUea meUea

Kile Kile

treatments. treatments.

residual residual

spatial spatial

ways ways

root root

genets, genets,

A. A.

species species

to to

from from

by by

in in

surrounding surrounding

may may

insect insect

result result

and and

testing testing

risk risk

Different Different

not not

rhizomorphs, rhizomorphs,

Armillaria Armillaria

behavior behavior

colonization colonization

A. A.

different different

access access

a a

under under

populations populations

appears appears

Bruhn Bruhn

suitable suitable

of of

occupied occupied

same same

often often

forest forest

decline. decline.

genet's genet's

or or

the the

and and

due due

genets genets

even-aged even-aged

(1989) (1989)

are are

co-occurring co-occurring

and and

1997; 1997;

explaining explaining

affect affect

the the

modeling modeling

influenced influenced

it it

as as

example, example,

each each

result result

of of

Rizzo Rizzo

gallica gallica

a a

sole sole

of of

slopes slopes

retum retum

inhibited inhibited

belonging belonging

preference. preference.

by by

gallica gallica

the the

of of

long-term long-term

in in

as as

al. al.

1994). 1994).

other's other's

distrtbutions distrtbutions

of of

may may

highest highest

that that

boundaries boundaries

of of

A. A.

can can

in in

For For

and and

Armillaria Armillaria

same same

A. A.

different different

Armillaria Armillaria

meUea meUea

genet. genet.

can can

et et

fungi, fungi,

unexpected unexpected

meUea meUea

had had

silvicultural silvicultural

side side

Thus, Thus,

fungal fungal

size size

Our Our

host host

1996; 1996;

the the

the the

perhaps perhaps

producer producer

A. A.

Armillaria Armillaria

resources resources

in in

each each

the the

representative representative

meUea meUea

A. A.

including including

genets genets

experimental experimental

genet genet

1992, 1992,

with with

or or

interactions interactions

occupy occupy

with with

larger larger

the the

al. al.

within within

of of

of of

isolation isolation

of of

Guillaumin Guillaumin

A. A.

1995), 1995),

activity activity

discussion, discussion,

and and

Bruhn Bruhn

al. al.

have have

small small

projections projections

potential potential

meUea meUea

interested interested

communities communities

et et

MOFEP MOFEP

sites. sites.

structure, structure,

base base

contact. contact.

tabescens tabescens

inhibited inhibited

within within

small small

genets. genets.

1997) 1997)

et et

operations operations

plots, plots,

only only

prolific prolific

among among

with with

strategies strategies

contrtbutions contrtbutions

tabescens tabescens

A. A.

and and

conditions, conditions,

their their

A. A.

are are

The The

within within

species species

species species

species species

(e.g., (e.g.,

resources resources

genets genets

above above

influence influence

A. A.

food food

west-facing west-facing

three three

overlap overlap

forest forest

virulence virulence

gallica gallica

disease disease

genet genet

experimental experimental

Armillaria Armillaria

forest forest

being being

should should

(Leibold (Leibold

spatial spatial

we we

associated associated

that that

mapping mapping

genetic genetic

to to

field field most most

to to

or or

genet. genet.

and and

found found

study study

MOFEP MOFEP

of of

development development

gallica gallica

Smith Smith

Legrand Legrand

in in

the the

3 3

all all

of of

of of

A. A.

substrate, substrate,

species species

Larsen Larsen

reflect reflect

may may

base base

of of

relative relative

when when

root root

A. A.

and and

the the

the the

expressed expressed

(e.g., (e.g.,

interactions interactions

1993; 1993;

1991; 1991;

forest forest MOFEP MOFEP

sets sets

nents nents

Silvicultural Silvicultural

meUea meUea

tems tems

lected lected

meUea meUea

MOFEP MOFEP

mately, mately, involve involve

in in

interactions interactions ral ral decline decline

From From

(1997) (1997)

may may

south-

Armillaria Armillaria

food food

the the

commonly commonly

The The

gallica gallica

overlap overlap

same same

block block

access access

strategies strategies

gesting gesting

three three

colonization colonization

they they virulence. virulence.

ing ing

hardwood-specializing hardwood-specializing areas areas

far far

ences ences Mohammed Mohammed

Since Since

unique unique

frequent frequent

is is

Armillaria Armillaria

but but

without without

Armillaria Armillaria

when when

of of

1 1

on on

soil soil

of of

half half

A. A.

in in

less less

has has

three three

It It

A. A.

ex­

most most

slopes. slopes.

was was

vegeta­

species species

It It

for for

spread spread

on on

be be

south­

than than

sets sets

al. al.

interac­

sites. sites.

than than

the the

Ranch) Ranch)

on on

slope slope

elsewhere elsewhere

meUea, meUea,

meUea meUea

to to

rising rising

but but

blocks blocks

map map

to to

that that

site, site,

degrada­

communi­

genet genet

et et

warmer, warmer,

of of

of of

of of

site. site.

side side

on on

of of

rhizomorph rhizomorph

the the

Armillaria Armillaria

A. A.

A. A.

rhizomorph rhizomorph

MOFEP MOFEP

in in

because because

frequently frequently

rhizomorphs rhizomorphs

than than

treatment, treatment,

of of

no no

gallica gallica

frequently frequently

meUea meUea

silvicultural silvicultural

side side

rhizomorphs rhizomorphs

differences differences

dry dry

Peck Peck

differences differences

with with

of of

3 3

abundant abundant

layers. layers.

east-facing east-facing

slopes slopes

fewer fewer

MOFEP MOFEP

distrtbutions distrtbutions

for for

any any

or or

detected detected

A. A.

a a

A. A.

that that

the the

drier, drier,

robust robust

and and

few few

lignin lignin

forest forest

moist moist

pre-treatment pre-treatment

less less

to to

Studies Studies

no no

blocks blocks

few few

on on

affect affect

variety variety

of of

in in

were were

appears appears

at at

a a

of of

appears appears

(the (the

soil soil

maps maps

ELT, ELT,

among among

slopes slopes

the the

side side

rhizomorph rhizomorph

pattems pattems

belonging belonging

No No

but but

most most

(Donnelly (Donnelly

less less

3 3

little little

and and

perhaps perhaps

were were

especially especially

at at

strategies," strategies,"

was was

in in

0.2-ha 0.2-ha

can can

east-facing east-facing

on on

rich rich

2, 2,

soil soil

found found

rest rest

increase increase

three three

gallica gallica

be be

side side

floor floor

north-

ELT's ELT's

MOFEP MOFEP

to to

local local

silvicultural silvicultural

soil soil

upper upper

meUea meUea

meUea meUea

were were

and and

the the

west-facing west-facing

(especially) (especially)

generally generally

meUea meUea

A. A.

the the

Further, Further,

the the

conditions conditions

anticipate anticipate

genets genets

block block

detected detected

absence absence

distrtbution distrtbution

or or

the the

and and

the the

and and

in in

A. A.

distrtbutional distrtbutional

therefore therefore

3, 3,

of of

to to

A. A.

slopes. slopes.

gallica gallica

soils soils

1 1

A. A.

of of

drying drying

the the

to to

and and

in in

indicate indicate

by by

structure, structure,

are are

cellulose cellulose

forest forest

It It

each each

and and

study study

the the

of of

the the

detected detected

encountered encountered

distrtbution. distrtbution.

A. A.

with with

west-facing west-facing

was was

variables, variables,

or or

of of

3 3

within within

north-

1 1

than than

differences differences

plots plots

and and

180 180

em em

incomplete. incomplete.

to to

side side

plots. plots.

in in

generally generally

in in

temperature temperature

dependent dependent

to to

block block

depth, depth,

5 5

among among

forest forest

"colonization "colonization

that that

often often

that that

of of

em em

is is

gaUica gaUica

growth growth

south-

stand stand

west-facing west-facing

ELT ELT

blocks blocks

were were

three three

in in

effects, effects,

5 5

genet genet

plots. plots.

Armillaria Armillaria

gallica. gallica.

in in

represents represents

(1976) (1976)

A. A.

and and

em em

less less

to to

gallica gallica

on on

gallica gallica

rhizomorphs rhizomorphs

in in

Seasonal Seasonal

by by

blocks blocks

of of

gaUica gaUica

explained explained

rockier rockier

A. A.

Working Working

whereas whereas

would would

the the

is is

occurs occurs

reasonable reasonable

ubiquitous ubiquitous

south-

A. A.

upper upper

30 30

A. A.

ridgetop ridgetop

studied studied

the the

protected protected

occurring occurring

shown shown

shown shown

in in

is is

A. A.

detected detected

species species

assigned assigned

similar similar

or or

be be

sample sample

slope slope

plots plots

rates rates

(especially) (especially)

distrtbution distrtbution

among among

significant significant

upper upper

the the

west-facing west-facing

the the

south-

1990). 1990).

mellea mellea

overlap overlap

distrtbution distrtbution

than than

have have Our Our

treatment treatment

ties ties affected affected

tions tions

tion tion

seems seems

Morrison Morrison

in in posed posed

moisture moisture more more

sites, sites, tion tion

the the

growth growth

mellea mellea with with Armillaria Armillaria below below

been been

If If and/ and/

and and

either either

rhizomorph rhizomorph sites sites

plots plots

may may

growth. growth.

side side

detected detected

to to

differences differences The among among

distrtbution distrtbution both both of of

but but whereas whereas

Both Both

frequently frequently

blocks, blocks,

detected detected

either either

nearly nearly

were were where where /~' ~M©W~W------·------

uneven-aged management to the risk of declline Although Armillaria species are certainly not the are not clear. Comparisons of these two sys­ only organisms that contribute to mortality or tems from the standpoint of decline exacerba­ decline in the Ozarks, they are of particular tion should focus attention on the frequency of interest because of the spatial stability of stand entiy, the spatial and size distributions of Armillaria genets (i.e., their long-term relation­ stumps created (i.e., new Armillaria food bases), ship with forest structure), and their pivotal role the extent of forest floor disturbance, and in mediating the influences of stress events and aboveground residual tree damage. We are the activities of stress agents (Wargo 1996). documenting harvest effects on our study plots Other relevant organisms and diseases include by mapping and characterizing stumps, re­ oak wilt, Hypoxylon canker of oak, the two-lined sidual stem injuries, and vehicle paths. Below­ chestnut borer, and defoliating insects (e.g., the ground root damage along vehicle paths is also looper complex and gypsy moth). Oak wilt being characterized. Although root wounds are disease is widely distributed in the Ozarks not always necessary for host infection by A. (Jones and Bretz 1958). The oak wilt pathogen tabescens (Rhoads 1956), they have been found (Ceratocystis jagacearum) is a primary parasite to increase host vulnerability (Weaver 1974), capable of infecting and killing healthy oaks. probably in part because A. tabescens rhizo-­ Oak wilt is most severe in stands approaching morph growth through soil rarely if ever occurs. pure red oak species composition, where root It has also been shown that damaged roots are grafts connect a high proportion of the most more vulnerable to A. mellea invasion than susceptible trees (Bruhn et al. 1991). Because uninjured roots, and that this effect is not oak wilt epidemiology is independent of host limited to the point of injury (Popoola and Fox stress (at least with red oak species), oak wilt 1996). Root collar and basal stem injuries may and oak decline are not causally related. have similar physiological effects on host vul­ Hypoxylon canker of oak (caused by Hypoxylon nerability to Armillaria root disease and/ or butt atropunctatum) has been associated with other rot. Maps of the juxtaposition of stumps, factors causing oak decline and mortality vehicle paths, residual trees, and Armillaria (Bassett and Fenn 1984, Law and Gott 1987). genets will provide unprecedented opportunJlties Bassett and Fenn (1984) showed that the to interpret forest community dynamics. pathogen occurs in branches and boles of healthy oaks without causing disease until the Starkey et al. (1989) associated the risk of oak advent of stress; they were not able to cause decline in southem upland hardwood forests disease with artificial inoculations. They iso­ with acute summer drought, recent or repeated lated the pathogen with equal frequency from spring defoliation, stand maturity, predomi­ non-diseased branches and boles of healthy nance of red oak group species, low site index, black or red oaks and white oaks, suggesting and xeric site conditions. Dwyer et al. (1995•) that the greater observed incidence of disease found that oak decline in the Ozarks affected on black or red oaks was due to differences in stressed trees regardless of age. Nevertheless, susceptibility or exposure to drought. Although silvicultural options for maintaining healthy the two-lined chestnut borer (Agrilus bilineatus) stands are more satisfactory than options for is most often a secondary colonizer of severely dealing with declining ones. Partial cutting in stressed or dying trees, it can occasionally build declining stands for any reason often results in to population levels capable of accelerating acceleration of decline, and regeneration of mortality. Borer activity in the Ozarks is com­ declining stands can be complicated by the monly associated with formation of mortality impaired condition of trees needed as vigorous pockets in conjunction with oak wilt, Armillaria seed or sprout sources (Starkey et al. 1989). root disease, and/ or Hypoxylon canker (Law As species composition shifts away from the red and Gott 1987). Although the gypsy moth has oak group in declining stands, managers will not yet arrived in the Ozarks, a very high pro­ have to decide whether or not to augment portion of Ozark land area supports forest natural hardwood regeneration by encouragiing stands comprising very high densities of tree or planting shortleaf pine. In young high risk species preferred by the gypsy moth (Liebhold et stands prior to the advent of decline, partial al. 1997). cuttings may reduce stress and shift species composition toward more resistant species (e.g., It seems appropriate to close this consideration white oak, shortleaf pine, etc.). Shortening the of relevant Ozark forest pathogens and insect rotation age may reduce stand vulnerability to pests with a brief mention of annosus root decline if it reduces physiological stress levells. disease of shortleaf pine, caused by 268 Heterobasidion aruwswn. Once found widely Brookshire, Brian L.; Hauser, CarL 1993. The distrtbuted in the Ozarks (Beny and Dooling Missouri Forest Ecosystem Project. In: 1962), Heterobasidion aruwsum has become all Gillespie, Andrew R.; Parker, George R.; but forgotten with the encroachment of oaks Pope, Phillip E.; Rink, George; eds. Proceed­ onto logged-over upland Ozark pine forest sites ings, 9th central hardwood forest confer­ (Johnson and Law 1989) and the de-emphasis ence; 1993 March 8-1 0; West Lafayette, IN. on pine regeneration. A substantial portion of Gen. Tech. Rep. NC-161. St. Paul, MN: U.S. the Ozark land area currently supporting Department of Agriculture, Forest Service, black/scarlet oak forest was previously domi­ North Central Forest Experiment Station: nated by more drought-tolerant shortleaf pine 289-307. (Law and Gott 1987). Although annosus and Armillaria root diseases share some important Brookshire, B.L.; Jensen, R.; Dey, D.C. 1997. features (Sinclair et aL 1987), in the Ozarks The Missouri Ozark Forest Ecosystem annosus root disease does not noticeably affect Project: past, present, and future. In: hardwoods and pine is not appreciably affected Brookshire, Brian L.; Shifley, Stephen R., by ArmiUaria root disease. Although the distrt­ eds. Proceedings of the Missouri Ozark bution and intensity of annosus root rot in Forest Ecosystem Project symposium: an preceding pine forests are unknown, there are experimental approach to landscape re­ no records of "pine decline" corresponding to search; 1997 June 3-5; St. Louis, MO. Gen. more recent records of oak decline. It seems Tech. Rep. NC-193. St. Paul, MN: U.S. plausible that shortleaf pine is ecologically Department of Agriculture, Forest Service, better adapted to the more stressful upland North Central Forest Experiment Station: 1- Ozark sites than are members of the red oak 25. subgenus. Perhaps oak decline functions to shift forest vegetation on these sites toward Bruhn, J.N.; Brenneman, J.A.; Wetteroff, J.J., greater compatibility with the long-term local Jr.; Mihail, J.D.; Leininger, T.D. 1997. environment. Spatial pattems of ArmiUaria populations in the Walker Branch Watershed throughfall LITERATURE CITED displacement experiment, Tennessee, USA. In: Pallardy, Stephen G.; Cecich, Robert A.; Agresti, A. 1990. Categorical data analysis. Garrett, H. Eugene; Johnson, PaulS., eds. John Wiley and Sons. 558 p. Proceedings, 11th central hardwood forest conference; 1997 March 23-26; Columbia, Anderson, J.B.; Kohn, L.M. 1996. Clonality in MO. Gen. Tech. Rep. NC-188. St. Paul, MN: soilbome, plant-pathogenic fungi. Annual U.S. Department of Agriculture, Forest Review of Phytopathology. 33: 369-391. Service, North Central Forest Experiment Station: 49-57. Anderson, J.B.; Ullrich, R.C. 1982. Transloca­ tion in rhizomorphs of Armillaria mellea. Bruhn, J.N.; Mihail, J.D.; Pickens, J.B. 1994. Experimental Mycology. 6: 31-40. Spatial dynamics of Armillaria genets in red pine plantations established on hardwood Bassett, E.N.; Fenn, P. 1984. Latent coloniza­ sites in northem Michigan. In: Johansson, tion and pathogenicity of Hypoxylon M.; Stenlid, J., eds. Proceedings of the 8th atropunctatum on oaks. Plant Disease. 68: intemational conference on root and butt 317-319. rots of forest trees; 1993 August 9-16; Wik, Sweden, and Haikko, Finland. IUFRO Bauce, E.; Allen, D.C. 1992. Role of Armillaria S2.06.0 1. Swedish University of Agricultural calvescens and Glycobius speciosus in a Sciences: 460-469. sugar maple decline. Canadian Joumal of Forest Research. 22: 549-552. Bruhn, J.N.; Pickens, J.B.; Stanfield, D.B. 1991. Probit analysis of oak wilt transmis­ Beny, F.H.; Dooling, O.J. 1962. Fornes annosus sion through root grafts in red oak stands. on shortleaf pine in Missouri. Plant Disease Forest Science. 37: 28-44. Reporter. 46: 521-522. Chen, J.; Xu, M.; Brosofske, K.D. 1997. Micro­ climatic characteristics in the southeastem

269

~M@W~~------·------

~ ~

Dwyer, Dwyer,

Garrett, Garrett,

Gregory, Gregory,

Davidson, Davidson, Garraway, Garraway,

Donnelly, Donnelly,

Darmono, Darmono,

Clinton, Clinton,

270 270

Armillaria Armillaria

root root

Shaw, Shaw,

Forest Forest

ton, ton,

by by

SeiVice: SeiVice:

infection. infection.

bial bial

and and

disease. disease.

Armillaria Armillaria

medium. medium.

DC: DC:

209. 209.

moisture, moisture,

Ozarks. Ozarks.

C.G., C.G.,

basin. basin.

degradation degradation

Cromack, Cromack,

57: 57: 75: 75:

landscape landscape

Louis, Louis,

Sydowia.42: Sydowia.42:

influences influences

Missouri Missouri

Shifley, Shifley,

Forest Forest ment ment

Paul, Paul,

Canopy Canopy

Missouri Missouri

symposium: symposium:

1991. 1991.

1991. 1991.

1995. 1995.

1938. 1938.

1993. 1993.

their their

J.P.; J.P.;

69-75. 69-75.

683-695. 683-695.

Ecology. Ecology.

U.S. U.S.

scarlet scarlet

DC: DC:

disease. disease.

S.D. S.D.

B.D.; B.D.;

S.C.; S.C.;

III; III;

Station: Station:

MN: MN:

A A

Pathogenicity Pathogenicity

Differentiation Differentiation Ontogeny Ontogeny

Interfertility Interfertility

P.K.; P.K.;

C.G., C.G.,

SeiVice: SeiVice:

MO. MO.

Ecology. Ecology.

T.W.; T.W.;

R.W.; R.W.;

SeiVice, SeiVice,

M.O.; M.O.;

Stephen Stephen

Forest Forest

gap gap

reactions reactions

dendrochronological dendrochronological

Agric. Agric.

Cutter, Cutter,

U.S. U.S.

21-4 21-4

Kile, Kile,

Department Department

Joumal Joumal

Ozark Ozark

Ozarks. Ozarks.

Annals Annals

1956. 1956.

temperature, temperature,

K., K.,

meUea meUea

tabescens tabescens

U.S. U.S.

research; research;

Boring, Boring,

Rishbeth, Rishbeth,

in in

Gen. Gen.

Entry, Entry, oak oak

in in

III; III;

characteristics characteristics

Burdsall, Burdsall,

an an

Campbell, Campbell,

Agric. Agric.

20: 20:

Hiittermann, Hiittermann,

oak oak

Jr. Jr.

7. 7.

105-116. 105-116.

Department Department

G.A., G.A.,

122-135. 122-135.

Handb. Handb.

forest forest

Ecology Ecology

76-87. 76-87.

North North

Department Department

Kile, Kile,

74: 74:

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------

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Experiment Experiment

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Agriculture, Agriculture,

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Agriculture, Agriculture,

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Forest Forest

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~M©W~W------­

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Protect. Protect.

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