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THE EFFECTS OF THE PARASITIC PLANT CUSCUTA
GRONOVII ON THE MATING SYSTEM OF ITS HOST
PLANT, IMPA TIENS CAPENSIS

presented by

KATHERINE MARGARET LANDER

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THE EFFECTS OF THE PARASITIC PLANT C USC UTA GRONOVII ON THE
MATING SYSTEM OF ITS HOST PLANT, IMPA T IENS CAPENSIS

By

Katherine Margaret Lander

A THESIS

Submitted to
Michigan State University
in partial fulfillment of the requirements
for the degree of

MASTER OF SCIENCE
Department of Plant Biology

2007

ABSTRACT

THE EFFECTS OF THE PARASITIC PLANT C USC UTA GRONOVII ON THE
MATING SYSTEM OF ITS HOST PLANT, IMPA TIENS C APENSIS

By
Katherine Margaret Lander

Parasitic plants attach to other plants and obtain water, nutrients, and/or carbon
from their vascular systems, causing a variety of effects at the individual, population, and
community levels. These effects have been hypothesized to be similar to those of insect
herbivores, but few studies have tested this idea. In this study, I investigated the effects
of the parasitic plant Cuscuta gronovii on the growth, fitness, and mating system of one
of its host plants, Impatiens capensis. I also attempted to compare the effects of the
parasite to the effects of insect herbivores, but the herbivory levels in the experiment
were too low to make a valid comparison. Plants infested with C. gronovz'i were 21%
shorter than plants that were not infested, produced 27% fewer seeds, and produced a
greater proportion of self-pollinated seeds (0.95 compared to 0.84). Instead of comparing
their effects to those of all insect herbivores, parasitic plants might more appropriately be
compared to other organisms that also act as physiological sinks, such as gall-forming

insects and sap-sucking insects.

ACKNOWLEDGMENTS

I thank the Gross lab crew for help with my research in the field, especially Desiree,
Margaret Yancey, Natalie Lenski, and Pam Moseley. I thank Mark Hammond for his
assistance at the Field Lab. I thank Greg Kowaleski for permission to do any research I
wanted to at the Kellogg Forest (as long as it didn’t harm the trees). I thank Carol Baker
for keeping the Gross lab supplies so organized and easy to find. I thank my lab mates
for comments on proposals and papers, especially Emily Grman, Todd Robinson, Wendy
Mahaney, Chad Brassil, Tony Golubski, Kenneth Mulder, Greg Houseman, Rich Smith,
and Sarah Emery. I thank my committee members, Katherine Gross, Jeff Conner, and
Doug Schemske, for helpful suggestions on research design and comments on my thesis.
For financial support, I thank the Plant Biology Department, the Kellogg Biological
Station, Michigan State University Distinguished Fellowship, National Science
Foundation GK-12 Fellowship, and the T. Wayne and Kathryn Porter funds. I thank all
my friends at KBS, both summer and year-round, for the potlucks, volleyball games,
parties, game nights, Grey’s Anatomy and Veronica Mars nights, and everything else that
makes KBS a great place to live. And I thank Aaron for always being there and

understanding.

iii

TABLE OF CONTENTS

LIST OF TABLES ............................................................................................................... v
LIST OF FIGURES ................................. vi
INTRODUCTION ............................................................................................................... 1
Study system ............................................................................................................ 3
METHODS .......................................................................................................................... 5
Kellogg Forest field experiment .............................................................................. 6
Field Lab pot experiment ......................................................................................... 8
Data collection ......................................................................................................... 9
Data analysis .......................................................................................................... 10
RESULTS .......................................................................................................................... 12
Herbivory and parasitism levels ............................................................................ 12
Effects of parasitism and herbivory ....................................................................... 15
Path analysis.........................- ................................................................................. 20
Environmental conditions ...................................................................................... 23
DISCUSSION .................................................................................................................... 23
Mediators of parasitic plant impacts ...................................................................... 24
Parasitic plants vs. insect herbivores ..................................................................... 25
Future research ...................................................................................................... 26
APPENDIX A: SUPPLEMENTAL DATA ...................................................................... 28
APPENDIX B: SUPPLEMENTAL BIBLIOGRAPHY .................................................... 33
Arthropod galls ...................................................................................................... 34
Fungal endophytes ................................................................................................. 36
Fungal pathogens ................................................................................................... 37
Parasitic plants ....................................................................................................... 39
Sap-sucking insects ................................................................................................ 4]
LITERATURE CITED ...................................................................................................... 45

iv

LIST OF TABLES

Table 1. Standardized total, indirect, and direct effects of variables used in the path
analysis on CH and CL seed production ............................................................................ 23

Table 2. Number of surviving Impatiens capensis plants per week per treatment at the
Kellogg Forest (mean i standard error, n=5). Surveys were initiated on June 21; no
surveys were done on August 2 or between September 5 and October 1 .......................... 29

LIST OF FIGURES

Figure 1. Research sites and surrounding area near the Kellogg Biological Station in
Kalamazoo County, Michigan. Site A: Kellogg Forest (field experiment); Site B: Field
Lab (pot experiment); Site C: Turkey Marsh (1. capensis collection site). Scale: 1 em =
0.72 km ................................................................................................................................ 6

Figure 2. Weekly estimates of % leaf area consumed by insect herbivores (mean :t
standard error, n = 6 groups of 9 plants per treatment) for I. capensis plants grown in pots
at the Field Lab The three treatments were significantly different from each other in the
second week, as indicated by the asterisk (*) .................................................................... 13

Figure 3a. Weekly estimates of the number of coils of C. gronovii on the stem of
parasitized I. capensis plants grown in pots at the Field Lab in the parasitism treatment
(mean i standard error, n = 6 groups) ................................................................................ 14

Figure 3b. The number of I. capensis plants parasitized by C. gronovii at the Field Lab in
the parasitism treatment over the growing season (mean :t standard error, n = 6 groups).
............................................................................................................................................ 15

Figure 4a. Final height (mean +/- standard error, n=6) of I. capensis plants measured at
the end of the season (September). Treatments with different letters are significantly
different at alpha=0.05 using Fisher’s LSD test ................................................................ 16

Figure 4b. Final biomass (mean 3: standard error, n=6) of I. capensis plants measured at
the end of the season (September). Treatments with different letters are significantly
different at alpha=0.05 using Fisher’s LSD test ................................................................ 17

Figure 4c. Total number of seeds produced (mean i standard error, n=6) by I. capensis
plants measured as the number of fruits and pedicels remaining on the plants at the end of
the season multiplied by the mean number of seeds per fruit. Treatments with different
letters are significantly different at alpha=0.05 using Fisher’s LSD test ........................... 18

Figure 4d. Proportion of cleistogamous (self-pollinated) seeds produced (mean i
standard error, n=6) by I. capensis plants measured as the number of CH and CL fruits
and pedicels remaining on the plants at the end of the season multiplied by the mean
number of seeds per each type of fruit and converted to a proportion. Treatments with
different letters are significantly different at alpha=0.05 using Fisher’s LSD test ............ 19

Figure 5. Initial path analysis model showing the hypothetical relationships between
biotic and abiotic factors, vegetative plant characteristics, and reproductive characteristics
of the host plant I. capensis. The arrows leading directly from light and parasitism to CH
and CL seeds represent any effects that are not mediated through height and biomass.

vi

The correlations between the dependent variables are through their residual error terms
(El-E4) ............................................................................................................................... 21

Figure 6. Path analysis model showing the hypothetical relationships between biotic and
abiotic factors, vegetative plant characteristics, and reproductive characteristics of the
host plant I. capensis. Line thickness represents the standardized regression weights.
Dashed lines indicate negative regression weights; solid lines indicate positive regression
weights. The proportion of variation in each variable explained by the model is indicated
by the numbers on the tops of the boxes of the dependent variables. The asterisks to the
left of the lines represent the significance level: *** p<0.01, ** 0.01<p<0.05, *
0.05<p<0.1. GFI = 0.982 .................................................................................................. 22

Figure 7. The % leaf area consumed by insect herbivores per plot per week (mean i
standard error, n=5) for 1. capensis plants grown in the Kellogg Forest ........................... 29

Figure 8a. The number of leaves with damage from insect herbivores per group per week
(mean i standard error, n=5) for I. capensis plants grown in the Kellogg Forest ............. 30

Figure 8b. The number of leaves with damage from insect herbivores per group per week
(mean 1 standard error, n=6) for I. capensis plants grown at the Field Lab ...................... 30

Figure 9a. The number of leaves per plant per plot per week (mean 1: standard error, n=5)
for I. capensis plants grown in the Kellogg Forest ............................................................ 31

Figure 9b. The number of leaves per plant per group per week (mean i standard error,
n=6) for I. capensis plants grown at the Field Lab ............................................................ 31

Figure 10a. The height per plant per plot per week (mean i standard error, n=5) for I.
capensis plants grown in the Kellogg Forest ..................................................................... 32

Figure 10b. The height per plant per group per week (mean i standard error, n=6) for I.
capensis plants grown at the Field Lab .............................................................................. 32

vii

INTRODUCTION

Parasitism is ubiquitous in plant communities (Dobson and Hudson 1986).
Though they are often overlooked in ecological theory and practice, parasites have been
shown to have large effects on communities and ecosystems by influencing the course of
succession (Van der Putten et a1. 1993), altering host life history traits (Clay 1986), and
altering species composition in communities (Weste and Marks 1987). While the effects
of some groups of parasites on plant communities have been well-studied, (e. g.,
nematodes [De Rooij-Van der Goes 1995], viruses [Malmstrom et a1. 2005], and fungi
[Holah and Alexander 1999]), the ecological effects of parasitic plants on other plants in
the community have not received as much attention (Marvier 1998).

Parasitic plants have been hypothesized to have similar effects on host plants and
communities as those of herbivorous insects (Atsatt 1977, Pennings and Callaway 2002).
Like insect herbivores, parasitic plants have host preferences, alter host physiology and
morphology, and can reduce host fitness by reducing survival or reproductive output. In
a recent review, Pennings and Callaway (2002) compared the effects of parasitic plants
with herbivores. They reported that there are similarities in the effects of parasitic plants
and insect herbivores on host communities, including evidence that herbivores and
parasitic plants both can alter the competitive hierarchy of a plant community. There are
also important differences between parasitic plants and insect herbivores that may impact
how they affect plant communities. One important difference is that many insect
herbivores are mobile and parasitic plants are not. Mobile insects are able to move about
the landscape to find high quality food, while parasitic plants are more restricted in space,

with many species being confined to the same host plant throughout their entire life cycle

(i.e., mistletoes). While insect herbivores are more common across the landscape,
parasitic plants can have significant effects on plant population- and community-level
processes where they are found. Many questions about the similarities and differences
between insect herbivores and parasitic plants still remain unanswered and unstudied.

For instance, a plant’s mating system, the proportion of self-fertilized to out-
crossed seeds produced, is one of its important life history characteristics. A shift in the
mating system of a population of plants can affect the fitness of individuals
(Charlesworth and Charlesworth 1987) and the genetic variation within the population
(Hamrick and Godt 1990). A plant can be highly outcrossing, highly selfing, or have a
mixed mating system that produces both selfed and outcrossed seeds. In a survey of 345
plant species, Goodwillie et al. (2005) reported that 42% have a mixed mating system,
which they defined as having an outcrossing rate between 0.2 and 0.8. Plants achieve a
mixed mating system by self-pollinating ovules by anthers in the same flower, by
receiving pollen that was distributed by a pollinator from another flower on the same
plant (geitonogamy), or by producing heteromorphic flowers (some that are cross-
pollinated and some that are self-pollinated).

While several studies have reported the effects insect herbivores can have on a
plant’s mating system (Elle and Hare 2002, Steets and Ashman 2004, Cole and Ashman
2005, Ivey and Carr 2005), there are no reported studies of the effects of a parasitic plant
on its host’s mating system. Herbivory has been shown to impact a plant’s mating
system in several ways. Herbivores can directly impact plants by reducing their size or

the resources available for reproduction (Koptur et al. 1996), or indirectly affect a plant’s

fitness by causing it to produce smaller flowers that are less attractive to pollinators
(Strauss et al. 1996), resulting in a greater proportion of flowers being self-pollinated.
Study system

The Impatiens capensis-Cuscuta gronovii host-parasite system was used in this
study to compare the impacts of parasitic plants and insect herbivores on the growth,
fitness, and mating system of the host. Impatiens capensis is a native annual that is
commonly found in mesic habitats at the edges of wetlands, alongside rivers and lakes, in
moist woods, and in roadside ditches throughout the Midwestern and Eastern United
States. It produces both chasmogamous (CH) flowers that are open and cross-pollinated,
and cleistogamous (CL) flowers that are closed and self-pollinated. The dimorphic
flowers can be distinguished from each other as buds, flowers, fruits, and pedicels. Taller
plants produce significantly fewer CL flowers than shorter plants, but biomass has been
reported to have no effect on the proportion of CL flowers produced (Lu 2002). Seeds
from CH flowers require 1.5 to 2 times the investment of energy and resources as CL
seeds (Waller 1979), but seedlings germinated from CH seeds are competitively superior
to seedlings from CL seeds (Waller 1984).

Environmental conditions, such as light availability and soil moisture, can alter
the number and proportion of CH and CL flowers produced by an individual plant
(Schemske 1978, Waller 1980). Biotic factors can influence the mating system of I.
capensis as well. Steets and Ashman (2004) and Steets (2005) showed that herbivory
affects the mating system of I. capensis by reducing the resources available for
reproduction, shifiing the proportion of CL to CH flowers in favor of the less expensive

CL flowers. CL flowers are also advantageous in an uncertain environment because it

generally takes less time for a CL flower to complete development from a bud to a fruit
than it takes a CH flower (Schemske 1979).

A biotic factor that affects I. capensis that has not yet been studied in the context
of its mating system is the parasitic plant C uscuta gronovii, which is commonly a parasite
of I. capensis. While C. gronovii is not a specialist on I. capensis, Schoolmaster (2005)
reported that in some habitats C. gronovii must infect I. capensis as a seedling before it
can infect any other host species. In Michigan, C. gronovii germinates from seeds in the
soil in early June, but withers and dies within a few days if it does not make contact with
a suitable host plant. Once its haustoria penetrate a host plant, the connection to the soil
withers, and C. gronovii grows entirely aboveground for the rest of its life cycle, sinking
coils of haustoria into the stem and petioles of the host plant. The more coils the parasite
produces around a plant, the more severely the fitness of the plant is affected. In one
study in which individuals of the host plant Hormathophylla spinosa, a woody shrub,
with 10%, 30%, 60% and 100% of the canopy covered with C uscuta epithymum were
surveyed, host plants with more than 60% of their surface covered with produced
significantly fewer seeds than host plants with less than 30% covered (Gomez 1994).

The Impatiens capensis-Cuscuta gronovii host-parasite system is an ideal system
to investigate parasitic plant-host plant interactions and compare the effects of a parasite
with the effects of insect herbivores for several reasons. First, I. capensis and C. gronovii
commonly co-occur in wetlands and disturbed mesic habitats in southwest Michigan.
Second, it is simple to distinguish self-pollinated fruits from cross-pollinated fruits in I.
capensis. Third, I. capensis is fed upon by a variety of herbivorous insects. Fourth, it is

easy to quantify parasitism by C. gronovii because it is a shoot parasite and grows

entirely aboveground. In addition, because I. capensis is an annual and does not have a
seed bank in the soil (Leck 1979), it is possible to determine the fitness effects of
herbivory and parasitism in a single growing season

I used this system to address two questions: 1. Does the parasitic plant C. gronovii
alter the growth, fitness, and mating system of its host I. capensis? and 2. How do the
effects of the parasite compare to the effects of insect herbivores? I hypothesized that
parasitic plants would have more severe effects on the host plants in terms of growth,
fitness, and mating system than herbivores because parasitic plants are constantly
associated with a host throughout the season and as a consequence may reduce resources
to the host more than herbivores do.

METHODS

I conducted two experiments to compare the effects of insect herbivores and
parasitic plants on the mating system of I. capensz's: a field experiment to examine the
effects of herbivory and parasitism in a natural population, and a more controlled pot
experiment using transplanted seedlings grown within a fence to exclude deer, which
often feed on and trample I. capensis plants (personal observation). Both experiments
were designed to test the direct effects of herbivory and parasitism independently, but not
their interaction, and included three treatments: herbivory, parasitism, and control. The
plants assigned to the herbivory treatment were subjected to natural levels of insect
herbivory and no parasite was introduced. The plants assigned to the parasitism
treatment were sprayed with insecticide and one parasite individual was introduced per
plot or group of plants. The plants assigned to the control treatment were sprayed with

insecticide and no parasite was introduced.

Kellogg Forest field experiment
I established the field experiment in an area of the Kellogg Forest along the bank
of Augusta Creek in Kalamazoo County, Michigan (Figure 1, Site A) with a relatively
uniform distribution of I. capensis in the understory. I selected fifteen 1 m2 plots in an

area where the dominant vegetation was comprised of I. capensis and randomly assigned
each plot to one of three experimental treatments (herbivory, parasitism, or control) with
5 plots per treatment. I selected thirty I. capensis plants in each plot and monitored them

for growth and reproductive characteristics (see Data collection, below).

Kellogg Biological Station

 

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Figure 1. Research sites and surrounding area near the Kellogg Biological Station in
Kalamazoo County, Michigan. Site A: Kellogg Forest (field experiment); Site B: Field
Lab (pot experiment); Site C: Turkey Marsh (1. capensis collection site). Scale: 1 em =
0.72 km

The plots were established in a location where none of the I. capensis plants
growing in this area in the previous year had been parasitized by C. gronovii, although
patches of C. gronovr'i were located nearby. To introduce the parasite to the plants in the
parasitism treatment, I collected seeds from the Kellogg Forest in fall 2005, germinated
them in the greenhouse and then added them to the parasitism treatment plots in early
June when C. gronovr'r' was observed germinating naturally in the Kellogg Forest. To
stimulate germination, I soaked the seeds in concentrated sulfirric acid for 30 minutes,
rinsed them under running water for 5 minutes, and then placed them on damp filter
paper in Petri dishes that were kept in the greenhouse for two weeks. Within a few days
of germination, I tied one C. gronovr'i individual with cotton thread to an I. capensis
individual at the center of each parasitism treatment plot. Several failed to establish
within a week, so I replaced them with cuttings from C. gronovz'i individuals growing
naturally in the Kellogg Forest.

I attempted to reduce insect herbivory in the control and parasitism treatments by
spraying the plots assigned to those treatments with insecticide every 7-14 days as
needed. I used two insecticides in combination: Conserve (Dow AgroSciences, 5 mL per
gallon of water) to reduce herbivory by caterpillars and Endeavor (Syngenta, 1 gram per
gallon of water) to reduce herbivory by aphids and whiteflies. These two insecticides
have been shown to have no impact on I. capensis grth or reproduction (Steets 2005).
I sprayed the herbivory treatment with water at the same time to control for the addition
of water to the control and parasitism plots.

There was a great deal of mortality of the I. capensis plants in the field

experiment due to deer herbivory and trampling. Only 50% of the Kellogg Forest plants

survived to the end of July. The parasitic plant C. gronovir' also failed to establish in all
but one of the plots at the Kellogg Forest. As a result, I did not analyze data from this
experiment, but instead used the observed biotic and abiotic characteristics as a
comparison for the plants grown in pots at the Field Lab. Data from the Kellogg Forest
plants are summarized in Appendix A.
Field Lab pot experiment

To establish the pot experiment at the Field Lab (Figure 1, Site B), I collected I.
capensis individuals from a natural population growing at the edges of Turkey Marsh, a
wooded wetland area at the Kellogg Biological Station (Figure 1, Site C). Seedlings were
collected when they were 15 to 25 cm tall and transplanted into pots (diameter: 16 cm,
height: 14 cm) filled with potting soil. I planted a single individual in the center of each
pot and arrayed them in groups of nine pots inside a fenced deer-exclosure at the Kellogg
Biological Station’s Terrestrial Plant Ecology Field Lab. The pots were placed under a

shade cloth that was open at the sides to allow insect (pollinator and herbivore) access.

The shade cloth reduced the photosynthetically active radiation levels from 1778 pE/mz/s

in full sun to a mean of 600 uE/mz/s, which is similar to the light availability in some

areas of the Kellogg Forest.

I used groups of 9 pots to create conditions more similar to the natural conditions
that would allow the parasite to spread from the center plant in the group to the other
plants in the group. It was necessary to have several pots in a group because the parasite
C. gronovz'i needs to have access to several host individuals as it matures or it drains too
many resources from one plant and kills it (personal observation). Groups of pots were 1

meter apart from each other to prevent the parasite from spreading to adjacent groups.

Once the experiment was established, 1 could not move the pots again because the
parasitic plant grew across individuals in the groups. As a consequence 1 could not
randomize effects of environmental variation that occurred under the canopy. I
randomly assigned the groups of pots to the three treatments (control, herbivory, or
parasitism), with 6 replications per treatment. To maintain soil moisture at levels similar
to those in natural populations, the plants were watered every morning by a sprinkler for
20 minutes.

I introduced the parasite in the parasitism treatment by tying one individual of C.
gronovii, germinated as described above, to the center plant in the group of 9 pots. The
parasite eventually established in all of the parasitism treatment replications at the Field
Lab. I reduced herbivory in the control and parasitism treatments using insecticides as
described above.

Data collection

I monitored growth, reproduction, and herbivory and parasitism levels on all
plants in both experiments at weekly intervals for 12 weeks. I measured growth as height
and number of leaves. I measured the percent herbivory by scoring the proportion of area
missing from each leaf to the nearest 10%, and then calculated the mean percent
herbivory for the entire plant. I measured parasitism levels as the number of coils of C.
gronovz’r' around each I. capensis plant. At the height of fruiting, CH and CL fruits were
collected from a subset of the plants so that the mean number of seeds per fruit could be
calculated, and then for each plant multiplied by the number of fruits produced. In late
September, the aboveground biomass of all surviving plants were harvested, dried at 60

0C for 5 days, and weighed. Before I harvested each plant, I counted the number of fruits

still on the plant and the number of pedicels remaining from fruits that had already
dehisced to determine the total fitness of each plant.

Light and soil moisture levels were determined in both experiments at the
beginning of September. I measured the photosynthetically active radiation (PAR) at
solar noon i 1 hour on successive cloudless days using a Sunfleck PAR Ceptometer
(Decagon) at the top of the I. capensis canopy. I calculated the percent water content as
the mean of three measurements taken in the center of each plot or pot using a TDR
probe (Trime).

Data analysis

To test the effects of the treatments (parasitism, herbivory, and control) on the
dependent variables height, biomass, total seed production, and proportion CL seed
production, I conducted a single-factor ANOVA on the group means of all surviving
plants using SAS (Version 9.1). Because not all nine plants in the parasitism treatment
groups became parasitized during the season, non-parasitized individuals were excluded
from the group mean of this treatment.

All plants in the herbivory treatment experienced some level of herbivory during
the season. To test for differences in the weekly estimates of herbivory level among the
three treatments, I used a repeated measures test in SAS (Version 9.1) using PROC GLM.

Because the groups of pots could not be moved once the experiment was
established, the variation in light availability due to proximity to the edge of the shade
cloth could not be controlled. To model the relationships of the effects of the parasitic
plant and the effects of light availability on I. capensis reproduction, a path analysis using

AMOS (Version 6.0) was conducted on data from the control and parasitism treatments.

10

From a review of the literature, I expected that light availability would be
important in determining the amount of reproduction and the balance between CH and
CL reproduction (Schemske 1978, Waller 1980). I used light level (PAR) recorded over
the canopy of each group of 9 pots and the means of height, biomass, CH seeds, and CL
seeds for all surviving plants of the groups of 9 pots measured at the end of the season for
the path analysis. CH and CL seeds were calculated by collecting a subset of mature
fruits from all treatments, then multiplying the numbers of fruits and pedicels from
dehisced fruits to obtain an estimate of total seed production over the season for each
plant. Parasitism was included in the model as the mean total number of coils per group
per week.

I included several correlations in the model. 1 expected plant height and biomass
to be correlated because taller plants would have more leaf nodes and branches and thus
more mass. 1 included both height and biomass in the path analysis because I. capensis
plants need to achieve a certain height before they are able to produce CH flowers (Lu
2002), regardless of biomass. I also expected a correlation between CH and CL seeds; it
could be a positive correlation because larger plants produce more of each seed type, or it
could be a negative correlation if larger plants switch to producing primarily CH seeds.

Many indices can be used to evaluate the fit of the model for a path analysis. I
looked at the following: the goodness of fit index (GFI), the comparative fit index (CFI),
and the root mean square of error approximation (RMSEA). All three indices indicated

the same results, so I only report the GFI.

11

RESULTS
Herbivory and parasitism levels

Several orders of insects were observed feeding on I. capensis over the course of
the experiment, including Lepidoptera (caterpillars), C oleoptera (beetles), Homoptera
(aphids), and Hemiptera(p1anthoppers). In this study, 1 only quantified the amount of
herbivory done by the chewing insects (Lepidoptera and Coleoptera), not the sucking
insects (Homoptera and Hemiptera). However, herbivory levels by chewing insects were
low (on average less than 1% of each plant was damaged) in the experiment. Only
during one week were herbivory levels significantly higher in the herbivory treatment
than in the control and parasitic treatments (Figure 2).

In the parasitism treatment, the mean number of coils per parasitized plant per
group increased throughout the season (Figure 3a). The number of plants that were
parasitized in each experimental unit ranged from 3 to 9, with a mean of about 5 plants by
the end of the season (Figure 3b). By the end of the season, the number of coils per

parasitized plant ranged from 2 to 107.

12

2.5

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— o- - Control
- -I - -+ Herbivores‘
——t—— + Parasites

% Herbivory
5‘.

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1-Jul 11-Jul 21-Jul 31-Jul 10- 20- 30— 9-Sep 19-
Aug Aug Aug Sep
Date

Figure 2. Weekly estimates of % leaf area consumed by insect herbivores (mean i
standard error, n = 6 groups of 9 plants per treatment) for I. capensis plants grown in pots
at the Field Lab. The three treatments were significantly different from each other in the

second week, as indicated by the asterisk (*).

13

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1-Jul 21-Jul 10-Aug 30-Aug 19—Sep

Date

Figure 3a. Weekly estimates of the number of coils of C. gronovii on the stem of
parasitized I. capensis plants grown in pots at the Field Lab in the parasitism treatment
(mean :t standard error, n = 6 groups).

14

 

 

 

 

 

# plants parasitized

 

 

1-Jul 21 -Jul 10-Aug 30-Aug 19-Sep
Date

Figure 3b. The number of I. capensis plants parasitized by C. gronovii at the Field Lab in
the parasitism treatment over the growing season (mean i standard error, n = 6 groups).

Effects of parasitism and herbivory
Parasitism by C. gronovii had significant effects on several attributes of I.
capensis growth and reproduction, but herbivory did not have a significant impact on any

of these characteristics (Figure 4). Significant treatment effects were found for height

(F235 = 9.03, p = 0.003), biomass (F115 = 3.87, p = 0.044), seed production (Fst = 4.01,
p = 0.040), and proportion of CL reproduction (F 2,15 = 18.52, p <0.0001). Fisher’s LSD

test showed that in all cases the parasitism treatment was significantly different from the

control and herbivory treatments, which did not differ from each other.

15

60

 

 

 

 

 

 

 

 

 

 

 

 

A A
50 T
I L B
40 j
A .l.
E
3
E 30
or
'6
I
20
10
O 3'
Control + Herbivores + Parasites

Figure 4a. Final height (mean +/- standard error, n=6) of I. capensis plants measured at
the end of the season (September). Treatments with different letters are significantly
different at alpha=0.05 using Fisher’s LSD test.

16

 

 

 

Biomass (g)
0.)

 

 

 

 

 

 

 

 

 

 

Control + Herbivores + Parasites

Figure 4b. Final biomass (mean i standard error, n=6) of I. capensis plants measured at
the end of the season (September). Treatments with different letters are significantly
different at alpha=0.05 using Fisher’s LSD test. _

l7

500 A

400 T

 

 

 

 

 

 

 

 

 

 

 

 

 

“’ l
i
I.- -b
3 300 B
i r
3 200 J_

100

0
Control + Herbivores + Parasites

Figure 40. Total number of seeds produced (mean i standard error, n=6) by I. capensis
plants measured as the number of fruits and pedicels remaining on the plants at the end of
the season multiplied by the mean number of seeds per fi'uit. Treatments with different
letters are significantly different at alpha=0.05 using Fisher’s LSD test.

18

_ 7“", '77

7’1!

 

 

 

 

 

 

 

 

 

 

 

 

 

a
0.95 T
i i
m
g 0.9 A
U, s
l,
('5' T A g
g 0.85 l
'e i T l
8- I
2 0.8
o.
l
0.75
0.7
Control + Herbivores + Parasites

Figure 4d. Proportion of cleistogamous (self-pollinated) seeds produced (mean :t
standard error, n=6) by I. capensis plants measured as the number of CH and CL fruits
and pedicels remaining on the plants at the end of the season multiplied by the mean
number of seeds per each type of fruit and converted to a proportion. Treatments with
different letters are significantly different at alpha=0.05 using Fisher’s LSD test.

19

Path analysis
The path analysis model (Figure 5) was consistent with the data (x2 = 0.576, df =

1, p = 0.448, n=12). This model was constructed such that the arrows leading directly
from light and parasitism to CH and CL seeds represent any effects that are not mediated
through height and biomass.

This model explains 98% of the variation in CL seeds and 97% of the variation in
CH seeds. The effect on reproduction is mediated by height and biomass, of which 41%
and 11% respectively of the variation is explained by light and parasitism (Figure 6). CH
and CL seed production were affected to similar degrees by parasitism (Table 1). Height

affected CH seeds more strongly than CL seeds, as expected.

20

 

 

 

Light

 

 

 

Height

 

\a

 

 

 

 

CH seeds

 

 

A

(9%

6
/ .

 

Parasitism

 

 

 

 

 

 

 

Biomass

 

 

 

 

CL seeds

 

O

Figure 5. Initial path analysis model showing the hypothetical relationships between
biotic and abiotic factors, vegetative plant characteristics, and reproductive characteristics
of the host plant I. capensis. The arrows leading directly from light and parasitism to CH
and CL seeds represent any effects that are not mediated through height and biomass.
The correlations between the dependent variables are through their residual error terms

(El-E4).

2]

—-_—1r

 

.‘fli‘ L

 

ODD-0.19
0.20-0.39

 

 

 

 

 

L' ht — 0.40-0.59 P , ,
rg 0.50-0.79 arasrtrsm

 

 

 

 

 

To. — 0.80-1.00
I

x ** “\

 

I

I

I

I

I

I

I

I

I

\ s '
\l :
I

I

I

I

I

I

I

I

I

I

I

 

i .I 0.42 0.11 x 1
Biomass

 

 

 

 

 

 

‘ ‘ ***

 

 

 

0.97 0.98‘

 

  

CH seeds CL seeds

@ fir

’
-----——-———‘

 

 

 

Figure 6. Path analysis model showing the hypothetical relationships between biotic and
abiotic factors, vegetative plant characteristics, and reproductive characteristics of the
host plant I. capensis. Line thickness represents the standardized regression weights.
Dashed lines indicate negative regression weights; solid lines indicate positive regression
weights. The proportion of variation in each variable explained by the model is indicated
by the numbers on the tops of the boxes of the dependent variables. The asterisks to the
left of the lines represent the significance level: *** p<0.01, ** 0.01<p<0.05,

* 0.05<p<0.1. GFI = 0.982.

22

Table 1. Standardized total, indirect, and direct effects of variables used in the path
analysis on CH and CL seed production.

 

Variable Total effects Indirect effects Direct effects
On CH seeds

Height 0.427 0.427
Biomass 0.601 0.601
Parasitism -0.432 -0.436 0.004
Light 0.047 -0.179 0.132
On CL seeds

Height 0131 -0.l31
Biomass 1 .084 1.084
Parasitism -0.325 -0.261 0064
Light 0115 -0.064 0052

Environmental conditions
Although the shade treatment reduced light availability in the pot experiment to
levels similar to those in the Kellogg Forest and the pots were watered daily, the Kellogg
Forest was both wetter and shadier than the Field Lab site. Soil moisture levels ranged
from 16.3% to 26.2% in the pots at the Field Lab with a mean of 21.9%, which were well

below levels at the Kellogg Forest (44.0% to 91.6% with a mean of 70.0%).

Photosynthetically active radiation (PAR) ranged from 149 to 727 pE/mZ/s at the Field
Lab under the shade cloth with a mean of 608.7 uE/mz/s; one group of 9 pots (at the edge
of the shade cloth) received close to full sunlight at noon (1741 uE/mz/s). At the Kellogg

Forest, PAR ranged from 20 to 659 uE/mz/s, with a mean of 209.5 uE/mz/s.

DISCUSSION
The results of this experiment show that parasitism by C. gronovr'i negatively
affects the growth, fitness, and mating system of its host I. capensis. However, I was not

able to compare the effects of parasitism to that of insect herbivores as initially proposed

23

due to low levels of insect herbivory at the Field Lab and high levels of deer herbivory
and lack of parasite establishment at the Kellogg Forest.

While the insect herbivory levels observed in this study were low, they were not
unprecedented for woodland herbaceous plants. Steets and Ashman (2004) surveyed 10
populations of I. capensis in Pennsylvania during one season and found that the mean
proportion of leaves damaged (leaves with any herbivore damage/total leaves) ranged 1

from about 0.15 to 0.45. When calculated this way, the herbivory levels of the plants in

 

the herbivory treatment at the Field Lab ranged from 0.009 to 0.11 across the season.

The number of leaves damaged each week stayed fairly constant (mean = 2 leaves), but
these plants produced so many leaves (more than 1000 leaves for some plants by the end
of the season) that the herbivory levels were nearly undetectable. The herbivory levels in
the Kellogg Forest ranged from 0.13 to 0.37 over the season, with a mean of 0.26, which
is consistent with the levels reported by Steets and Ashman (2004).

Insect populations have been observed to be extremely variable through time
(Turchin 1990) and many species experience episodic outbreaks following years of low
abundance. These outbreak cycles have been shown to affect reproductive output in
populations of perennial plants (Carson and Root 2000). In annuals, an episodic outbreak
could cause a complete reproductive failure and in a species like I. capensis, with no seed
bank, this would result in local extinction. It is unclear if the low levels of insect
herbivory observed at the Field Lab are typical of this site.

Mediators of parasitic plant impacts
In this study, parasitism of Impatiens capensis by C uscuta gronovii resulted in a

significant reduction in total reproduction, and in the proportion of outcrossed (CH,

24

chasmogamous) seeds produced. In addition, the path analysis revealed that these
reductions in host plant fitness were mediated through the effects of parasitism on plant
height and biomass. There was no significant direct effect of parasitism on CH and CL
seed production, indicating that there was no additional effect of parasitism on fitness
beyond the effects mediated through the reductions in height and biomass. The model
explained less of the variation in height and biomass, indicating that factors other than
parasitism and light are involved in determining these traits (e.g., unmeasured
environmental or soil factors).

Parasitic plants vs. insect herbivores

The extremely low levels of herbivory in this experiment prevent direct
comparisons of the effects of parasitism and herbivory on I. capensis. However, the
magnitude of the parasitism effects I measured is higher than those reported by Steets and
Ashman (2004). I found that the parasitic plant C. gronovii reduced height by 21%,
compared to the 10% reduction by insect herbivores found by Steets and Ashman (2004).
The reduction in total reproduction was also stronger (27% by the parasite, compared to
14% by insects [Steets and Ashman 2004]). In this study, parasitism increased the
proportion of CL seeds from 0.84 to 0.95; in Steets and Ashman (2004), herbivory
increased the proportion of CL seeds from 0.57 to 0.70.

Based on these comparisons, parasitism had stronger effects on plant growth and
reproduction than insect herbivory did, contrary to some of the predictions of Pennings
and Callaway (2002). While both herbivory and parasitism levels are likely to vary
spatially and temporally, once an area has been colonized by a parasite I would expect

that the effects would be strong and consistent across years (unless the parasite or host go

25

 

locally extinct). Thus the abundance of the host and parasite are more likely to be
coupled in time. Predictions of the effects of parasitic plants on host plants will need to
incorporate these differences in spatial-temporal dynamics.

The mobility and mode of feeding of an insect herbivore may also impact its
effects on fitness. Sap-sucking insects (e. g., aphids) that tend to colonize a host at low

numbers, increase over time, and stay on the host for a long time may have comparable

‘ A. 1'

effects on fitness to parasitic plants. The aphid stylets might function similarly to

parasitic plant haustoria and cause a physiological drain on the host. Gall-forming

 

Vt.

insects, such as the gall fly Eurosta solidaginis which produces galls on goldenrod, could
also act as physiological sinks and would be expected to have effects comparable to those
of parasitic plants. I have compiled a bibliography of research papers with data on the
impacts of different types of insects on host plants that could be used to explore these
effects (Appendix B).
Future research

Research in this area could have several possible future directions. One possible
approach would be to repeat this study in a year or across sites with higher levels of
insect herbivory. Treatments in which herbivores were intentionally introduced could
also be used to better quantify the effects of varying levels of herbivory on plant fitness
and then used to compare to a range of parasitism levels.

To investigate the long-term effects that C. gronovii has on I. capensis
populations, communities with C. gronovii could be surveyed over several years to
determine whether C. gronovii always parasitizes plants in the same spatial areas, as l

have observed, or whether it follows plants around the habitat (Callaway and Pennings

26

1998). Genetic analyses could also be done to determine if C. gronovii prefers to
parasitize inbred plants derived from CL seeds or plants from outcrossed CH seeds. It
would be interesting to know whether populations of I. capensis that are consistently
parasitized by C. gronovii have different outcrossing rates than populations that have not
been recently parasitized. I would expect that because C. gronovii increases the
proportion of selfed (CL) seeds produced by I. capensis that parasitized populations
would have a lower outcrossing rate. However, if C. gronovii prefers to parasitize plants
from outcrossed CH seeds, spatial cycles could result.

Finally, Schoolmaster (2005) observed that C. gronovii uses 1. capensis as a nurse
plant, meaning that the parasite needs I. capensis to establish, but it conducts most of its
reproduction on nearby perennial plants. In this experiment, the parasite did not have the
option of parasitizing other species of plants, and so this may have magnified the impacts
on I. capensis reproduction. In natural populations of I. capensis, the parasite may move
onto other species (e. g., Onoclea sensibilis, Solidago patula, Eupatorium maculatum) as
it grows and this may limit (or reduce) its impact on I. capensis. Thus the impact of the
parasite on I. capensis populations may vary more in sites with alternative hosts (e.g.,
diverse wetlands) than where I. capensis forms a monoculture (e.g., the Kellogg Forest

site).

27

 

 

APPENDIX A: SUPPLEMENTAL DATA

This appendix contains data on vegetative characteristics of I. capensis
populations from the Kellogg Forest field experiment and Field Lab pot experiment (see
Methods and Data collection, above). Seeds were not counted from I. capensis fruits
harvested in the Kellogg Forest, so there are no data on total reproduction for plants from
this site. Data for the Kellogg Forest plants are presented as mean values per plot of the
surviving plants (see Table 2 for population density data). Plants whose tops were eaten
by deer but still survived with some leaves lower on their stems are excluded from the
graphs because they would skew the measurements of height and numbers of leaves.
Data for the Field Lab plants are presented as mean values per group of 9 plants. The
graphs are plotted with the same scale on the y-axes for the Kellogg Forest and the Field
Lab.

The treatments are defined as follows: The plants assigned to the herbivory
treatment were subjected to natural levels of insect herbivory and no parasite was
introduced. The plants assigned to the parasitism treatment were sprayed with insecticide
and one parasite individual was introduced per plot or group of plants. The plants
assigned to the control treatment were sprayed with insecticide and no parasite was

introduced.

28

Table 2. Number of surviving Impatiens capensis plants per week per treatment at the
Kellogg Forest (mean :1: standard error, n=58). Surveys were initiated on June 21; no

surveys were done on August 2 or between Se

)tember 5 and October 1.

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Week Date Control Herbivory Parasitism
l June2l 30i0 303:0 30i0
2 June 28 29.2 i 0.2 29 :t 0.45 29 a: 0.45
3 July 5 19.8 d: 3.2 22.4 dc 2.18 20.2 :t 1.93
4 July 12 17.2 d: 3.60 20 i 2.59 18.8 :t: 1.74
5 July 19 17.5i2.72 18i2.51 16:t 1.97
6 July 26 17.25 i 2.87 17.4 i 2.42 15.4 i 2.16
8 August 9 15.25 i 3.54 15.4 :t 1.81 14 :t 2.35
9 August 16 15.25 :t 3.54 15.4 $1.81 13.2 i 2.52
10 August 23 14.75 :1: 3.82 14.4 i 1.86 12.8 i 2.56
11 August 30 14.75i 3.82 13.4i 1.63 12.2i2.l8
12 September 5 14 :l: 3.56 12.2 i 1.66 11.6 i 1.66
15 October 1 6 :l: 1.96 5.8 i 1.62 5.4 i 0.93

 

an=4 for the control treatment after July 12 due to destruction of one plot by deer.

 

°/o Herbivory
(a)

 

 

 

 

0

17-Jun

15-Jul

12-Aug
Date

9-Sep

 

 

— 9- -Control
- -l - -Herbivory
+Parasitism

 

Figure 7. The % leaf area consumed by insect herbivores per plot per week (mean :1:
stande error, n=5) for I. capensis plants grown in the Kellogg Forest.

29

 

 

 

— o— - Control

- -I - -Herbivory
—*:7Parasitism

 

 

# of leaves damaged by herbivory

 

   

 

O I I I I J
17-Jun 15—Jul 12-Aug 9—Sep 7-Oct

Date

Figure 8a. The number of leaves with damage from insect herbivores per group per week
(mean :t standard error, n=5) for I. capensis plants grown in the Kellogg Forest.

(.0

 

 

— o- - Control
- -I - -Herbivory
+ Parasitism

 

 

 

 

# of leaves damaged by herbivory

 

 

 

0 I l I I If T I I

1-Jul11-Jul21-Jul31-Jul 10- 20- 30— 9—Sep 19-
Aug Aug Aug Sep

Date

Figure 8b. The number of leaves with damage from insect herbivores per group per week
(mean :1: standard error, n=6) for I. capensis plants grown at the Field Lab.

30

 

500 ~

400«

 

— o- - Control

- -I - -Herbivory
——n.— Parasitism
200 4 I

3004

 

 

 

Number of Leaves

 

100 r
L,

- .—'. r.‘

 

 

 

 

O -
17-Jun 15-Jul 12-Aug 9—Sep 7-Oct

Date

I I T T

Figure 9a. The number of leaves per plant per plot per week (mean i standard error, n=5)
for I. capensis plants grown in the Kellogg Forest.

 

 

 

 

 

 

 

 

500 —
3 400 «
>
8
.r — o— - Control
.. 300 ~ .
E - -I - -Herbrvory
g +Parasitism
200 -
E
a
Z
100 «
o .
1-Jul 11-Jul 21—Jul 31-Jul 10- 20- 30- 9-Sep 19-
Aug Aug Aug Sep
Date

Figure 9b. The number of leaves per plant per group per week (mean i standard error,
n=6) for I. capensis plants grown at the Field Lab.

31

 

90
80 _
70 ~

— .- -Corfirflorfi

- -I - -Herbivory
+Parasitism

60*

 

50~

 

Height (cm)

40—

30]

 

 

 

20 T ‘r . ,
17-Jun 15-Jul 12-Aug 9-Sep 7-Oct
Date

Figure 10a. The height per plant per plot per week (mean i: standard error, n=5) for I.
capensis plants grown in the Kellogg Forest.

90 -———-——— ~——

 

80—

70‘

      

— + - Control
- -I - -Herbivory
+ Parasitism

 

 

Height (cm)

50‘ iii
40— J

l
605 |
l
l
i
30« ’

 

20 I l T I I I I l
1-Jul 11-Jul 21-Jul 31-Jul 10- 20- 30- 9-Sep 19-
Aug Aug Aug Sep
Date

 

Figure 10b. The height per plant per group per week (mean :1: standard error, n=6) for I.
capensis plants grown at the Field Lab.

32

APPENDIX B: SUPPLEMENTAL BIBLIOGRAPHY
Pennings and Callaway (2002) hypothesized that parasitic plants are similar to
insect herbivores in their effects on plant populations and communities. However, many
insects chew the leaves of plants and then move onto new hosts, whereas parasitic plants
tap into the xylem and phloem of a plant and so act as continual physiological sinks on

the host plants. These two types of organisms might be expected to have different effects 5
on plant survival and reproduction because they operate in fundamentally different ways. i
I

It is also likely that the way in which an herbivore feeds on a host plant would affect its

 

effect on plant growth and fitness. Based on this, 1 proposed that instead of comparing
parasitic plants to all insect herbivores, the effects of parasitic plants should be compared
to those groups of organisms that also act as continual physiological sinks on plant
resources: sap-sucking insects (Hemiptera), gall-forming insects (larvae of several
orders), and fungal endophytes and pathogens.

I compiled literature containing data of the effects of these organisms on their
host plants by Using the following search string in ISI Web of Science in July 2006: (sap-
sucking OR sap-feeding OR parasitic plant“ OR galls OR galling OR gall OR fungus or
fungal) AND (host OR biomass OR growth OR reproduction OR herbivory) NOT
genetic. I added papers that contained data in graph or tabular form to the bibliography.
To obtain any papers that I missed in this search, I looked through each paper’s literature
cited section to obtain older papers, and I found newer papers that cited each paper using
181 Web of Science. In the end, I compiled 26 papers on arthropod galls, 11 papers on
fungal endophytes, 24 papers on fungal pathogens, 26 papers on parasitic plants, and 28

papers on sap-sucking insects. Several papers contain data from more than one species

33

within a taxa (i.e., two species of aphids were studied) or measure the effects on more
than one species of host plant, so these papers would generate multiple data points in a
meta-analysis.

The following list of papers contains data in tables or graphs of the effects of the
above-listed taxa on host plant growth or reproduction. This data could be used to
conduct a meta-analysis to determine whether parasitic plants have similar effects on
their hosts as any of the other taxa.

Arthropod galls

Abrahamson, W. G., and K. D. McCrea. 1986. Nutrient and biomass allocation in

Solidago altissima: effects of two stem gallmakers, fertilization, and ramet
isolation. Oecologia 68: 174-180.

Boydston, R. A., and M. M. Williams. 2004. Combined effects of Aceria malherbae and
herbicides on field bindweed (Convolvulus arvensis) growth. Weed Science
52:297-301.

DeClerck-Floate, R., and P. W. Price. 1994. Impact of a bud-galling midge on bud
populations of Salix exigua. Oikos 70:253-260.

Dhileepan, K., and R. E. C. McFadyen. 2001. Effects of gall damage by the introduced
biocontrol agent Epiblema strenuana (Lep., Tortricidae) on the weed Parthenium
hysterophorus (Asteraceae). Journal of Applied Entomology-Zeitschrift Fur
Angewandte Entomologie 125 : 1-8.

Erasmus, D. J ., P. H. Bennett, and J. Van Staden. 1992. The effect of galls induced by the
gall fly Procecidochares utilis on vegetative grth and reproductive potential of
crofton weed, Ageratina adenophora. Annals of Applied Biology 120: 173-181.

Fay, P. A., and D. C. Hartnett. 1991. Constraints on growth and allocation patterns of

Silphium integrifolium (Asteraceae) caused by a cynipid gall wasp. Oecologia
88:243-250.

Fay, P. A., D. C. Hartnett, and A. K. Knapp. 1996. Plant tolerance of gall-insect attack
and gall-insect performance. Ecology 77:521-534.

Fay, P. A., and H. L. Throop. 2005. Branching responses in Silphium integrifolium

(Asteraceae) following mechanical or gall damage to apical meristems and
neighbor removal. American Journal of Botany 92:954-959.

34

Femandes, G. W., A. F. L. Souza, and C. F. Sacchi. 1993. Impact of a Neolasioptera
(Diptera: Cecidomyiidae) stem galler on its host plant, Mirabilis linearis
(N yctaginaceae). Phytophaga 5: 1-6.

Gonzales, W. L., P. P. Caballero, and R. Medel. 2005. Galler-induced reduction of shoot
growth and fruit production in the shrub Colliguaja integerrima (Euphorbiaceae).
Revista Chilena De Historia Natural 78:393-399.

Hakkarainen, H., H. Roininen, and R. Virtanen. 2005. Negative impact of leaf gallers on
arctic-alpine dwarf willow, Salix herbacea. Polar Biology 28:647-651.

Hoffmann, J. H., F. A. C. Irnpson, V. C. Moran, and D. Donnelly. 2002. Biological
control of invasive golden wattle trees (Acacia pycnantha).by a gall wasp,

Trichilogaster sp. (Hymenoptera: Pteromalidae), in South Africa. Biological
Control 25:64-73.

 

Ito, M. 2005. Effect of gall formation by a cynipid wasp, Andricus symbioticus, on the
development of the leaves and shoots of Quercus dentata. Entomological Science
82229-234.

Kloppel, M., L. Smith, and P. Syrett. 2003. Predicting the impact of the biocontrol agent
Aulacidea subterminalis (Cynipidae) on growth of Hieracium pilosella
(Asteraceae) under differing environmental conditions in New Zealand.
Biocontrol Science and Technology 13:207-218.

Larson, K. C., and T. G. Whitham. 1991. Manipulation of food resources by a gall-
forming aphid: the physiology of sink-source interactions. Oecologia 88:15-21.

Larson, K. C., and T. G. Whitham. 1997. Competition between gall aphids and natural

plant sinks: plant architecture affects resistance to galling. Oecologia 109:575-
582.

McCrea, K. D., W. G. Abrahamson, and-A. E. Weis. 1985. Goldenrod ball gall effects on
Solidago altissima: l4C translocation and growth. Ecology 66:1902-1907.

Navie, S. C., T. E. Priest, R. E. McFadyen, and S. W. Adkins. 1998. Efficacy of the stem-
galling moth Epiblema strenuana Walk. (Lepidoptera: Tortricidae) as a biological

control agent for ragweed parthenium (Parthenium hysterophorus L.). Biological
Control 13:1-8.

Preus, L. E., and P. A. Morrow. 1999. Direct and indirect effects of two herbivore species
on resource allocation in their shared host plant: the rhizome galler Eurosta

comma, the folivore T rirhabda canadensis and Solidago missouriensis. Oecologia
119:219-226.

35

Sacchi, C. F., and E. F. Connor. 1999. Changes in reproduction and architecture in
flowering dogwood, Cornusflorida, after attack by the dogwood club gall,
Resseliella clavula. Oikos 86: 138-146.

Sacchi, C. F., P. W. Price, T. P. Craig, and J. K. Itami. 1988. Impact of shoot galler attack
on sexual reproduction in the arroyo willow. Ecology 69:2021-2030.

Silva, I. M., G. I. Andrade, G. W. Femandes, and J. P. L. Filho. 1996. Parasitic
relationships between a gall-forming insect T omoplagia rudolphi (Diptera:
Tephritidae) and its host plant (Vernonia polyanthes, Asteraceae). Annals of
Botany 78:45-48.

Throop, H. L., and P. A. Fay. 1999. Effects of fire, browsers and gallers on New Jersey

tea (C eanothus herbaceous) growth and reproduction. American Midland
Naturalist 141:51-58.

Tooker, J. F ., and L. M. Hanks. 2006. Tritrophic interactions and reproductive fitness of
the prairie perennial Silphium laciniatum Gillette (Asteraceae). Environmental
Entomology 35:537-545.

Vuorisalo, T., M. Walls, and H. Kuitunen. 1990. Gall mite (Eriophyes laevis) infestation
and leaf removal affect growth of leaf area in black alder (Alnus glutinosa) short
shoots. Oecologia 84:122-125.

Weis, A. E., and A. Kapelinski. 1984. Manipulation of host plant development by the
gall-midge Rhabdophaga strobiloides. Ecological Entomology 92457-465.

Fungal endophytes

Cheplick, G. P. 2004. Recovery from drought stress in Lolium perenne (Poaceae): Are
fungal endophytes detrimental? American Journal of Botany 91 :1960-1968.

Cheplick, G. P., and R. Cho. 2003. Interactive effects of fungal endophyte infection and

host genotype on growth and storage in Lolium perenne. New Phytologist
158:183-191.

Cheplick, G. P., A. Perera, and K. Koulouris. 2000. Effect of drought on the growth of
Lolium perenne genotypes with and without fungal endophytes. Functional
Ecology 14:657-667.

Clay, K. 1987. Effects of fungal endophytes on the seed and seedling biology of Lolium
perenne and F estuca arundinacea. Oecologia 73:358-362.

Faeth, S. H., M. L. Helander, and K. T. Saikkonen. 2004. Asexual Neotyphodium
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