ORIGINAL PAPER

Decline of Cornus florida and forest successionin a Quercus–Carya forest

Aaron R. Pierce Æ William R. Bromer ÆKerry N. Rabenold

Received: 19 July 2006 / Accepted: 29 March 2007 / Published online: 21 April 2007

� Springer Science+Business Media B.V. 2007

Abstract Cornus florida is a common understory

species in many hardwood forests in eastern North

America. It plays an important role in nutrient cycling

and is an important food resource for many vertebrate

species, especially migratory birds. We used data

collected over a 16-year period to examine population

dynamics of a tagged population of C. florida in a

6.4 ha area in the context of change in the protected

Quercus–Carya forest of the Ross Biological Reserve,

Indiana. We examined the hypothesis that forest

dynamics result from interactions between long-term

ecological succession and pathogens. The C. florida

population at the Ross Reserve declined by 50%

between 1983 and 2000, with a survivorship of 24%.

Analysis of 40 years of forest survey data showed that

Quercus and Carya populations declined in impor-

tance, while Acer saccharum increased dramatically.

This change in forest structure is consistent with

successional changes occurring throughout the Mid-

west and can be attributed to suppression of distur-

bance. Cornus florida declined more sharply where A.

saccharum increased. From 1983 to 1999, C. florida

were less likely to survive if they were within 5 m of a

A. saccharum. Light measurements showed that A.

saccharum abundance correlated negatively with light

available to C. florida, suggesting that increased

shading by A. saccharum contributed to C. florida

decline. The fungus, Discula destructiva causes the

disease dogwood anthracnose that is associated with

widespread decline of C. florida in the eastern United

States. Tests for this pathogen in our study area were

mostly negative. Other tests revealed that Armillaria

root rot infected most C. florida, but this disease

seemed to be a secondary effect of shading by A.

saccharum. These results suggest that the lack of fire

and other anthropogenic disturbances has resulted in

an accelerated shift in dominance from Quercus and

Carya to A. saccharum in the main canopy, and this

shift, in turn, has resulted in increased shading of C.

florida and its decline in previously more open

Midwestern forests.

Kewords Cornus florida � Forest dynamics �Pathogens � Succession

Introduction

Cornus florida L. is a common understory tree

species of eastern North America, commonly found

A. R. Pierce � K. N. Rabenold

Department of Biological Sciences, Purdue University,

West Lafayette, IN 47907, USA

W. R. Bromer

Department of Natural Sciences, University of St. Francis,

Joliet, IL 60435, USA

Present Address:A. R. Pierce (&)

Department of Biological Sciences, Nicholls State

University, Thibodaux, LA 70310, USA

e-mail: aaron.pierce@nicholls.edu

123

Plant Ecol (2008) 195:45–53

DOI 10.1007/s11258-007-9297-6

in mesic and dry-mesic forests throughout the

Midwest (McLemore 1990). Cornus florida are most

prominent in second-growth areas that have been

recently disturbed by fire, logging, agriculture, or tree

falls (Muller 1982; Elliot et al. 1997). As hardwood

forests reach maturity, C. florida typically remains a

valuable understory species, forming a thin sub-

canopy layer (Terborgh 1985; Anagnostakis and

Ward 1996). Leaf litter produced by C. florida is

important in nutrient cycling, especially the rapid

return of calcium to surface horizons of the soil,

thereby buffering the soil against acidification

(Thomas 1969; Blair 1988; McLemore 1990). Cornus

florida is also an important food source for more than

40 species of birds and 12 species of mammals

(Bromer 1988; Stiles 1980). The C. florida fruit, that

ripens in the fall, has a high crude fat and lipid

content (Stiles 1980) making it an important high-

quality food source for neotropical migrants during

fall migration.

Recent research indicates that many C. florida

populations may be severely threatened throughout

their range (Sherald et al. 1996; Anagnostakis and

Ward 1996; Hiers and Evans 1997; Williams and

Moriarity 1999; Jenkins and White 2002; Holzmu-

eller et al. 2006). These declines have been

attributed the disease dogwood anthracnose caused

by the fungus Discula destructive (Redlin 1991;

Daughtrey et al. 1996). Dogwood anthracnose can

kill C. florida within 2 years and has caused

mortality rates of greater than 90% in some forests

(Erbaugh et al. 1995; Holzmueller et al. 2006).

Although C. florida declines have mainly been

attributed to dogwood anthracnose, other factors

may also be important to the decline of C. florida

in some stands, such as: (1) forest succession, (2)

pathogens other than dogwood anthracnose, (3)

insects, (4) disturbances such as wind storms or ice

storms, and (5) interactions between successional

dynamics and pathogens.

Forest succession is driven by disturbance,

changes in abiotic conditions, and interactions of

biotic factors that result in changes of composition,

structure, and biomass of vegetation (Barnes et al.

1998). Declining abundance of a species such as C.

florida may be a result of changing competitive

environments. For example, McEwan et al. (2000)

attributed a 36% decline in C. florida over a 10-

year period in an old-growth forest to canopy

closure and environmental stress. Successional

changes in species composition and abundance can

also affect microclimate conditions (Brown 1993;

Xu et al. 1997; Zheng 2000). Such changes could

initiate proliferation of new or dormant pathogens.

Numerous diseases are known to infect C. florida

(dogwood anthracnose, spot anthracnose, powdery

mildew, Armillaria root rot) and may also contrib-

ute to their decline.

Recent investigations at the Ross Biological

Reserve suggest a decline in the C. florida population

(Pierce et al. 2006). Thus, the first objective of this

study was to determine the magnitude of the C.

florida decline at the Ross Biological Reserve from

1983 to 1999. The second objective was to determine

the importance of three potential factors that may be

contributing to the decline of C. florida. Specifically,

we tested the hypothesis that C. florida have been

negatively affected by an increase in late successional

species and the habitat changes these species create.

We also determined if dogwood anthracnose was

associated with the C. florida decline. Finally, we

examined if interactions between the forest succes-

sional changes and Armillaria root rot were contrib-

uting to the decline of C. florida.

Methods

Study area

This study was conducted at the Ross Biological

Reserve, a 22 ha forest along the Wabash River in

Tippecanoe County, Indiana (408240 N 878040 W).

The Ross Biological Reserve has been divided into

40 · 40 m quadrats to provide a spatial framework

for various surveys conducted in the Reserve. It is

comprised of a mosaic of forest types due to

selective logging and grazing that occurred in the

early 1900’s. Since, Purdue University obtained the

land in 1949, no extensive disturbance has occurred,

resulting in a forest dominated by Quercus and

Carya species. The landscape is typified by gently

rolling plateaus with elevations ranging between

180 m and 150 m above sea level. Summer

temperatures average 228C and precipitation is

distributed fairly evenly throughout the year, aver-

aging 94 cm per year. Soils at the reserve range

from sandy loam to loamy fine sand.

46 Plant Ecol (2008) 195:45–53

123

Sampling design

We sampled C. florida in a 6.4 ha plot (comprised of

40 quadrats) in the Ross Reserve during the months

of June and August of 1983 (Bromer 1988) and

October and November of 1999. All C. florida greater

than 2.5 cm diameter at breast height (DBH) were

recorded, tagged, and mapped within this study plot.

The distribution of C. florida was plotted according to

size class ranging from 2.5 cm DBH to greater than

10.8 cm DBH in 2.1 cm DBH increments. Ingrowth

from one diameter class to another between studies

was calculated as the number of trees below a given

size class at the start of a measurement period that

entered another size class by the end of the

measurement period due to growth (Helms 1998).

Forest survey data on every individual tree of

every species (greater than 10 cm DBH) has been

collected every 10 years from 1960 to 2000 and were

used to examine the effects of forest succession

within the study plot on C. florida (Pierce et al. 2006).

In 2000, individuals greater than 4 cm DBH and less

than 10 cm DBH within a 2.56 ha sub-plot of the

6.4 ha C. florida study plot were also recorded, DBH

measured, and spatial distribution mapped. These

data were used to determine the influence of Acer

saccharum Marsh size and distance to nearest C.

florida on survival of C. florida individuals. For

methods and details of these data refer to (Pierce

et al. 2006).

During July 2001, light availability within the C.

florida plot was estimated by taking black and white

canopy photographs. All photographs were taken

between 10 am and 2 pm on sunny days during a two-

week period. Four equally spaced photographs were

taken from each quadrat with five or more C. florida

present (22 quadrats total). All photographs were

taken at a height of 7.5 m, using a telescoping pole, to

accurately estimate the light available to the C.

florida layer. The percent of open canopy was

determined by placing the photographs in an enve-

lope with 99 holes 2.5 mm in diameter, equally

spaced over the entire envelope surface, and counting

the number of open holes. Holes with 50% or more

open sky were scored as open and the percent of open

canopy was calculated from the ratio of open hole to

the total number of holes.

During the spring and summer of 2001, we

conducted three surveys in collaboration Gail Ruhl,

co-director of the Plant and Pest Diagnostic Labora-

tory at Purdue University, of every C. florida

(>2.5 cm DBH) within our C. florida study plot to

determine if any individuals were showing symptoms

of dogwood anthracnose, powdery mildew, or Armil-

laria root rot. Symptoms recorded included: brown

spots on leaves, gray or tan twigs with raised reddish-

brown spots, branch dieback, white mycelia on roots

and base of trunk, and rotten wood at the base of the

trunk. Samples of twigs and leaves were collected

from individuals suspected to be infected with

dogwood anthracnose. At the Plant and Pest Diag-

nostic Laboratory, samples were incubated at room

temperature for 24 h, and then viewed under a

microscope (40·) to examine for conidiomata that

resembled Discula destructiva. Samples with spores

within the size range of Discula destructiva spores

(6.0–13.0 · 2.5–4.0 lm) were sent to Dr. Scott

Redlin, Plant Pathologist at the USDA APHIS in

Raleigh, North Carolina for confirmation.

Data analysis

A Pearson correlation matrix was used to determine

the correlation between the abundance of selected

tree species in 2000 (>10 cm DBH), determined from

the forest survey, and the percent change in C. florida

abundance from 1983 to 1999. Species included in

the correlation matrix were based on their importance

within the forest and their changes in importance

since 1960, these included: Acer saccharum Marsh,

Quercus species, Carya species, Liriodendron tuli-

pifera L., Fraxinus species, and Junglans nigra L.

Correlation analysis was only performed on quadrats

with five or more C. florida in 1983 (22 of 40

quadrats). SAS Version 9.1 (SAS Institute Inc. 2004)

was used to calculate the correlation matrix.

A Pearson correlation matrix was also used to

determine the correlation between the abundance of

tree species in 2000, determined from the forest

survey and the C. florida survey, and percent of open

canopy, determined from the canopy photographs.

Species included in this correlation matrix were A.

saccharum, Quercus species, Carya species, L.

tulipifera, Fraxinus species, J. nigra, and C. florida.

A G-test for independence was used to determine if

survival of C. florida was independent of their

distance from A. saccharum (>10 cm DBH), based

on forest survey data (Pierce et al. 2006). A G-test for

Plant Ecol (2008) 195:45–53 47

123

independence was also used to determine if C. florida

with symptoms of disease infections was independent

of their distance from A. saccharum (>10 cm DBH).

Results

Descriptive statistics

In 1983, Bromer (1988) sampled and tagged 905 C.

florida (>2.5 cm DBH) in the C. florida study plot. In

the 16 years between surveys, there was a 50.7%

decline in the population (446 individuals >2.5 cm

DBH in 1999). Of the 446 C. florida present in 1999,

only 220 of them had been previously tagged in 1983.

Gross survivorship of C. florida over the 16-year

period was 24.3%. Although, overall survivorship

was low, some areas supported high C. florida

densities throughout the study.

The number of individuals in the two smallest

diameter classes (2.5–4.5 cm and 4.6–6.6 cm DBH)

decreased drastically over the 16-year period (Fig. 1).

Individuals in the 6.7–8.7 cm and 8.8–10.8 cm

diameter classes increased during the 16-year period

to 102 and 24 individuals, respectively. However, the

observed increase in these diameter classes was due

to ingrowth from smaller diameter classes over the

16-year period (Table 1). A total of 126 individuals

grew into larger diameter classes during the time

between surveys. The percent of total ingrowth was

highest among the larger diameter classes, showing

that most of the individuals in the large diameter

classes survived since 1983 and were not new

individuals. Survivorship of all diameter classes was

low, with the 6.7–8.7 cm diameter class having

highest survivorship at 37% and the lowest survivor-

ship occurring at both ends of the diameter class

spectrum (Table 1).

Forest succession

Forest data collected since 1960 (see Pierce et al.

2006 for methods and details) indicated a steady

decrease in the importance of the three major

Quercus (oak) and Carya (hickory) species at the

Ross Reserve (Table 2). Conversely, A. saccharum

consistently increased in importance from 8.10 in

1960 to 33.67 in 2000, moving up in rank from the

12th most important tree species to the 2nd most

important tree species at the Ross Biological Reserve.

In 2000, A. saccharum less than 10 cm and greater

than 4 cm DBH were the most abundant species

within the 2.4 ha sub-plot (a 16-quadrat sub-plot of

the C. florida plot). A. saccharum increased in

abundance from 981 individuals in 1983 to 1,259 in

2000. As well as becoming more abundant, A.

saccharum also became more important in the

canopy. In 1983, there were 22 A. saccharum greater

than 10 cm DBH, and by 2000 there were 265

individuals in this diameter class. Including all

diameter classes, there were 981 A. saccharum and

457 C. florida located within the sub-plot in 1983,

however, by 2000 there was a 28% increase in A.

saccharum and a 64% decrease in C. florida. The

decrease in C. florida was most conspicuous in parts

of the plot where A. saccharum increase was greatest.

The results of the Pearson correlation matrix

showed that only the abundance of A. saccharum in

2000 was negatively correlated with the percent

change in C. florida abundance (Table 3). The

abundance of L. tulipifera was also significantly

correlated with the percent change in C. florida, but

this was a positive correlation.

The percent of open canopy in each quadrat within

the C. florida plot ranged from 1% to 22.9%. The

Pearson correlation matrix based on the percent of

open canopy and tree species abundance resulted in

two species with a significant correlation (Table 3).

A. saccharum abundance had a negative correlation

0

50

100

150

200

250

300

350

400

450

500

2.5-4.5 4.6-6.6 6.7-8.7 8.8-10.8 >10.8

Size Class

1983 1999

fo ecnadnubA

.C

fadirol

Fig. 1 Total abundance of C. florida (>2.5 cm DBH) by

diameter class in 1983 and 1999 in the 6.4 ha C. florida plot at

the Ross Biological Reserve

48 Plant Ecol (2008) 195:45–53

123

with the percent of open canopy and the percent

change in C. florida had a positive correlation.

In 1999, 236 of the 398 C. florida within the

sapling plot that died since 1983 were within 5 m of a

A. saccharum greater than 10 cm DBH and only 28 of

the 136 live C. florida were within 5 m of a A.

saccharum greater than 10 cm DBH (Fig. 2). A G-test

of independence indicated a significant difference

Table 1 Diameter class (DBH in cm), survivorship, and ingrowth of C. floridas (>2.5 cm DBH) tagged in 1983 and resurvey in 1999

in our 6.4 ha study plot. The table does not include new individuals located in 1999

Size class 1983 1999 # Ingrowth % Ingrowth Survivorship (%)

2.5–4.5 431 12 – – 18.5

4.6–6.6 357 110 54 50.5 29.6

6.7–8.7 81 76 53 80.5 37.0

8.8–10.8 20 19 16 84.2 20.0

>10.8 16 3 3 100 0.0

Total 905 220 126

Table 2 Overstory forest dynamics at the Ross Biological

Reserve from 1960 to 2000 for selected tree species (based on

data from Pierce et al. 2006), including the number of stems/

ha, basal area (m2/ha), and rank based on importance value

calculated as the sum of the species relative density, relative

dominance, and relative frequency

Tree species 1960 1970 1980 1990 2000

Stems BA R Stems BA R Stems BA R Stems BA R Stems BA R

Quercus alba 90.2 1.66 1 93.9 1.86 1 100.9 2.09 1 76.1 1.85 1 64.6 1.81 1

Quercus velutina 38.1 0.84 2 39.8 0.94 2 28.9 0.81 2 21.9 0.67 3 19.1 0.65 4

Carya glabra 36.7 0.67 3 27.0 0.55 5 35.0 0.65 4 26.7 0.49 5 24.4 0.50 6

Fraxinus americana 28.0 0.53 4 30.6 0.64 3 31.5 0.79 3 27.2 0.76 2 23.0 0.71 3

Juglans nigra 22.6 0.48 5 23.5 0.53 4 21.9 1.97 5 17.2 2.06 6 15.2 2.15 7

Carya ovata 18.7 0.30 8 19.4 0.30 8 14.3 0.26 9 11.1 0.22 10 10.4 0.21 10

Quercus rubra 16.5 0.42 7 14.8 0.41 7 18.1 0.55 7 13.3 0.46 8 11.1 0.41 9

Liroidendron tulipifera 11.5 0.39 6 13.1 0.42 6 18.3 0.47 6 22.2 0.57 4 23.3 0.62 5

Carya cordiformis 9.6 0.12 9 16.1 0.21 9 21.9 0.31 8 16.1 0.25 11 13.5 0.24 11

Acer saccharum 6.3 0.11 12 7.2 0.13 10 13.0 0.21 10 32.6 0.40 7 68.9 0.80 2

Cornus florida 1.5 0.02 16 2.0 0.02 16 7.7 0.07 12 5.9 0.06 12 0.5 0.01 23

Table 3 Results of Pearson correlation matrix among the

abundance in 2000 of selected tree species and the percent

change in C. florida from 1983 to 1999 and the percent open

canopy in 2001 at the Ross Biological Reserve. Significant

correlations (Alpha < 0.05) are marked with an *

Species % Change in C. florida % Open canopy

Correlation P-value Correlation P-value

Quercus spp. 0.137 0.543 0.274 0.218

Carya spp. �0.050 0.826 0.093 0.681

Fraxinus americana �0.143 0.525 �0.081 0.719

Juglans nigra 0.072 0.752 0.215 0.336

Liroidendron tulipifera 0.452 0.035* 0.393 0.070

Acer saccharum �0.585 0.004* �0.777 <0.001*

% Change in C. florida – – 0.645 0.001*

Plant Ecol (2008) 195:45–53 49

123

(N = 534, df = 1, Gadj = 56.64, P < 0.001) in survival

of C. florida from 1983 to 2000 and distance to A.

saccharum, suggesting a link between proximity to A.

saccharum and C. florida survival.

Disease survey

No leaf spotting due to anthracnose was found within

the C. florida plot. Samples of leaves and twigs from

35 individuals that showed signs of dieback or stress

were collected in an attempt to isolate Discula

destructiva in the lab. Of these 35 individuals, only

one individual was found to be infected with Discula

destructiva.

Of the 446 C. florida alive in 1999, 86 had died by

2001 and seven new individuals were tagged for a

total of 367 living C. florida in 2001. Seventy-two of

the 86 dead C. florida had root rot mycelia growing

on the trunk or root system. Most of the live

individuals showed signs of stress, as 362 had branch

dieback and 121 had epicormic shoots. Also, 222 of

the live C. florida showed signs of root rot, with

mycelia growing on the root system or trunk and 68

of them had severe signs of root rot with rotten

trunks.

In 2001, the sapling plot contained 35 live C.

florida within 5 m of a large A. saccharum (greater

than 10 cm DBH). Of these 35 individuals, 26 were

infected with root rot. There were also 122 live C.

florida that were farther than 5 m from any A.

saccharum, and 64 of these were infected with root

rot. A G-Test of independence (Fig. 3) indicated a

significant difference in infection of root rot and

distance from large A. saccharum (N = 157, df = 1,

Gadj = 5.511, P = 0.02), suggesting a relationship

between root rot and proximity to A. saccharum.

Discussion

The C. florida population at the Ross Biological

Reserve has experienced a dramatic decline in

abundance over the 16 years of the study, and its

decline seems to be continuing with 19% of the

population dieing from 1999 to 2001. Conservative

estimates of the C. florida mortality rate over the

study period were extremely high (62%), recruitment

is very low, and the population does not appear

stable. The spatial variation in C. florida decline

provides clues concerning the causes of the decline.

0

50

100

150

200

250A

bund

ance

of

C.fl

orid

a

Dead Alive

Inside Outside

Fig. 2 Total abundance of live and dead C. florida (>2.5 cm

DBH) within 5 m of a A. saccharum (>10 cm DBH) and

outside a 5 m radius of A. saccharum. All individuals were

alive in 1983; those that died did so by 1999. G-test of

independence shows significant relationship (N = 534, df = 1,

Gadj = 56.64, P < 0.001)

0

10

20

30

40

50

60

70Root Rot No Root Rot

Inside Outside

Abu

ndan

ce o

f C

.flor

ida

Fig. 3 Total abundance of C. florida (>2.5 cm DBH) in 2001

infected with root rot and those not infected within 5 m of a A.saccharum (>10 cm DBH) and outside a 5 m radius of A.saccharum. G-test of independence shows significant relation-

ship (N = 157, df = 1, Gadj = 5.511, P = 0.02)

50 Plant Ecol (2008) 195:45–53

123

The successional shift in the forest community at

the Ross Biological Reserve is characterized by the

declining importance of the dominant Quercus and

Carya species and an increase in the importance of

shade-tolerant A. saccharum (Pierce et al. 2006). This

shift implicates competition, probably for light, as a

factor in the C. florida decline. The successional

pattern observed at the Ross Reserve is consistent

with patterns found throughout the region. Histori-

cally, Midwestern forests have been subject to

frequent disturbances including fire, timber harvest-

ing, grazing, and clearing for agricultural purposes.

Such land use practices have contributed to the

dominance of Quercus and Carya species (Crow

1988; Parker 1989; Abrams 1992; Shotola et al. 1992;

Goebel and Hix 1996). Since the early 1930’s,

however, the inception of forest management and

protection practices has resulted in fire exclusion in

many areas where fire facilitated the dominance of

oak forests (Shumway 2001). In the absence of fire

and other disturbances, many Quercus–Carya forests

have developed into A. saccharum-dominated forests

(Pallardy et al. 1988; Parker 1989; Abrams 1992;

Spetich and Parker 1998). The same pattern of

increasing importance of A. saccharum has occurred

at the Ross Biological Reserve (Pierce et al. 2006),

following a lack of disturbance at the site over the

past 50 years.

An increase in A. saccharum could have adverse

effects on the C. florida population because of

increased shading and competition for resources.

Although C. florida has been classified as very

tolerant of shade with maximum photosynthesis

occurring at one-third of full sunlight (McLemore

1990); the 14 quadrats in our study that showed at

least a 50% decline in C. florida had a mean percent

open canopy of less than 7%. In addition, there were

six quadrats that either showed no change or

increased in C. florida, these quadrats had a mean

percent open canopy of over 15%. The availability of

light has also been found to be more limiting to C.

florida than water or nutrient availability (Britton

1994). Due to earlier flushing of leaves in the spring,

shade-tolerant species such as A. saccharum and

Fagus grandifolia Ehrh. (American Beech) have a

greater adverse effect than Quercus species on

understory and middlestory species such as C. florida

(Barkman 1992). Horn (1971) found that more light

penetrates through an Quercus–Carya canopy than a

A. saccharum or F. grandifolia canopy. A. saccharum

and F. grandifolia develop leaves a month earlier

than oaks, producing shade for a greater period of

time. A. saccharum also produce denser shade due to

their oval shaped canopy; unlike Quercus species that

produce an irregular shape allowing more light to

reach the forest floor (Reisch et al. 1975).

As A. saccharum increased significantly beginning

in the 1980s, C. florida began to decline, and this

temporal association did not exist for other species of

canopy trees and C. florida decline. The correlation

analysis showing the relationship between change in

C. florida abundance and A. saccharum abundance

also indicated that C. florida were experiencing a

greater decline in abundance as a function of

increasing abundance of A. saccharum. The distance

to the nearest large A. saccharum in addition to A.

saccharum abundance also appears to have a negative

effect on C. florida abundance. The spatial associa-

tion between A. saccharum and C. florida mortality

did not exist for other canopy species.

It is likely that the importance of the distance from

A. saccharum to C. florida survival may be due to the

negative effect of A. saccharum on percent open

canopy and light available to C. florida. Percent of

open canopy was shown to be negatively related to A.

saccharum abundance and positively related to C.

florida abundance. C. florida farther away from A.

saccharum would have a greater chance of receiving

light penetrating through the forest canopy.

There were no widespread or apparent symptoms

of dogwood anthracnose in the C. florida population

at the Ross Biological Reserve. Thus, anthracnose

does not seem to be presently contributing signifi-

cantly to the C. florida decline at the reserve.

However, because there was a 16-year period

between surveys we cannot discount the possibility

that dogwood anthracnose moved through the popu-

lation during the time between surveys. In fact, the

mico-habitat conditions that have resulted because of

the continued increase of A. saccharum promote the

incidence and severity of dogwood anthracnose

(Chellemi and Britton 1992; McEwan et al. 2000;

Holzmueller et al. 2006). Nevertheless, the C. florida

population is not currently infected with dogwood

anthracnose but continues to decline, with 86 of the

446 C. florida dieing from 1999 to 2001, suggesting

that other factors are involved in the decline of this

population.

Plant Ecol (2008) 195:45–53 51

123

Besides anthracnose, there are other opportunistic

diseases that infect weakened or stressed trees. Since

forest succession is leading to increased shade levels

at the Ross Reserve, this could stress some understory

species making them more susceptible to disease.

Armillaria root rot is one disease that could take

advantage of a stressed C. florida population. Root rot

is opportunistic, infecting mostly ‘‘small or weak

individuals such as those shaded by taller plants’’

(Sinclair et al. 1993). The fungi causing root rot can

persist for decades in the soil, only becoming active

when an unhealthy host is available. Root rot, with

the help of other secondary pests and pathogens, will

kill an infected tree within 10–15 years (Sinclair et al.

1993). The high mortality of the Ross Reserve C.

florida population, the abundance of multiple signs of

stress, and the abundance of root rot infected

individuals indicate that the population is unhealthy.

The significant relationship between root rot and

proximity to A. saccharum suggests that A. saccha-

rum stressed the C. florida population; establishing a

link between successional change in the forest and

disease.

These results indicate that C. florida populations

may be threatened even in stands were dogwood

anthracnose is not present because of successional

dynamics and interactions with other native patho-

gens. Thus, management of C. florida may also be

necessary in stands not currently afflicted with

dogwood anthracnose in order to maintain healthy

and stable populations. Currently, prescribed burning

is the management technique that shows the most

promise in reducing the occurrence of dogwood

anthracnose (Holzmueller et al. 2006). Prescribed

burning would also be beneficial to C. florida in

forests similar to the Ross Reserve population. This

type of management would help maintain a dominant

Quercus–Carya component in the forests while

controlling the increase of A. saccharum and allevi-

ating the conditions that seem to be contributing to

the decline of C. florida even in forest not infected

with dogwood anthracnose.

Acknowledgments The Department of Biological Sciences

at Purdue University supported this project through the Ross

Biological Reserve. The following individuals helped to collect

data used for this study: R.A. Delanglade, H.J. Von Culin, S.

Austad, S. Wissinger, J. VanKley, E. Harris, and J. Winters.

We would also like to thank Dr. Gail Ruhl, Dr. Rick Howard,

Dr. George Parker, Dr. Sammy King, Dr. Dave Buckley, and

three anonymous reviewers for their valuable discussions and

reviews of this manuscript.

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