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The effects of biotic interactions on Ambrosia artemisiifolia L.
by
Arthur Andrew Meahan MacDonald
A Thesis submitted in conformity with the requirements
for the degree of Master of Science,
Graduate Department of Ecology and Evolutionary Biology,
List of Figures .......................................................................................................................vii
List of Tables........................................................................................................................viii
List of Tables........................................................................................................................viii
1 General Introduction .......................................................................................................1
1.1 Invasions.....................................................................................................................................................................1 1.1.1 Type of herbivore damage. .....................................................................................................................................3 1.1.2 Life history stage ....................................................................................................................................................4 1.1.3 Plant habitat ............................................................................................................................................................7
1.2 Native range studies are important..........................................................................................................................8
1.3 Study species ..............................................................................................................................................................8
2 The effects of disturbance and enemy exclusion on performance of Ragweed (Ambrosia artemisiifolia L.) at three life-history stages. ...................................................23
3.3 Results ......................................................................................................................................................................66 3.3.1 i) Direct effects of damage ...................................................................................................................................66 3.3.2 ii) Size-dependent effects .....................................................................................................................................66
3.4 Discussion.................................................................................................................................................................67 3.4.1 Weak effects of damage on plant performance .....................................................................................................68 3.4.2 Leaf clipping changes the pattern of allocation to biomass ..................................................................................70 3.4.3 Tolerance effects on invasions..............................................................................................................................71 3.4.4 Tolerance and the ERH.........................................................................................................................................72
4 General Discussion .......................................................................................................91
4.1 Summary of results .................................................................................................................................................91
4.2 Ambrosia and invasions ..........................................................................................................................................92 4.2.1 Ragweed in North America ..................................................................................................................................92 4.2.2 Ragweed’s Invasions ............................................................................................................................................93 4.2.3 Invasions in general ..............................................................................................................................................93
4.3 Suggestions for future work....................................................................................................................................94 4.3.1 Seeds.....................................................................................................................................................................94 4.3.2 Seedlings ..............................................................................................................................................................95 4.3.3 Mechanisms of tolerance and allocation...............................................................................................................95 4.3.4 Indirect effects of tolerance ..................................................................................................................................98
vii
List of Figures
Figure 2-1) Relationship between seed biomass and fecundity .............................................................. 42
Figure 2-2) Germinating seeds from samples of 10 seeds ...................................................................... 43
Figure 2-3) Seedling survivorship in response to herbivore exclusion treatments................................. 44
Figure 2-4) Damage to adult plants during the summer of 2007 ........................................................... 45
Figure 2-5) Damage to individual adult plants during the summer of 2008.. ........................................ 46
Figure 2-6) The incidence of stem-galling insects in 2008..................................................................... 47
Figure 2-7) Measures of plant performance in response to factorial field experiment in 2007. ............ 48
Figure 2-8) Measures of plant performance in response to factorial field experiment in 2008. ............ 49
Figure 3-1) Stem biomass in response to removal of leaves ................................................................... 74
Figure 3-2) Seed production in response to leaf removal ....................................................................... 75
Figure 3-3) The relationship between seed and plant biomass decreases with clipping damage ......... 76
Figure 3-4) Back-transformed elevations of the lines in Fig. 3-3 .......................................................... 77
Figure 3-5) The comparison of allometric reproduction between control and 75% damage................. 78
Figure 3-6) Seed mass in response to apical meristem clipping............................................................. 79
Figure 3-7) The relationship between seed and plant biomass not affected by apical removal. ........... 80
Figure 3-8) 95% confidence intervals for the regressions described in Fig 3-7 .................................... 81
Figure 4-1) A rough estimate of male flower mass ................................................................................ 99
viii
List of Tables
Table 2-1) A Table of the common enemies which occur on Ambrosia at our field site. ........................ 50
Table 2-2) ANOVA of enemy exclusion on seed germination.................................................................. 50
Table 2-3) ANOVA of enemy exclusion on seedling survival. ................................................................. 51
Table 2-4) Factorial ANOVA on the adult experiment in 2007.............................................................. 51
Table 2-5) Factorial ANOVA on the adult experiment in 2008............................................................... 52
Table 2-6) Proportion of plants surviving to reproduction in summer 2007 .......................................... 52
Table 2-7) Proportion of plants attacked by stem-galling insects in 2008. ............................................ 52
Table 3-1) Comparison of natural and simulated damage types ............................................................ 82
Table 3-2) ANOVA table for the linear model including plant size (stem biomass) as a continuous
variable and clipping as an ordered factor.. ........................................................................................... 83
Table 3-3)Parameter estimates (SE) for slopes and intercepts from the linear model of log(seed mass)
on log(stem mass). .................................................................................................................................. 83
1
1 General Introduction
1.1 Invasions
Human activities, particularly habitat alteration and the intentional and unintentional transport
of organisms, have caused rapid, unprecedented mixing of the Earth’s biota in a breakdown of what
Charles Elton (1958) called “Wallace’s Realms”: great biogeographic regions of distinctive, coadapted
organisms. While invasions do occur in nature, humans have accelerated that rate tremendously
(Vitousek et al. 1997) and are creating management crises that cost billions to control in the United
States (Pimentel et al. 2000, Mack et al. 2000) and in Canada (Colautti 2006). In particular, the
introduction of alien plant species has caused profound change in many now-threatened ecosystems
around the world with a concomitant loss of conservation, economic and aesthetic value. For example,
Bromus tectorum has altered the fire regime in North American grasslands and shrublands (Mack
1981), while Melaleuca quinquenervia has replaced entire areas of the Florida Everglades (Serbesoff-
King 2003). Invaded landscapes can be less economically productive: Leafy Spurge (Euphorbia esula)
prevents cow grazing in pastures (Leistritz et al. 1992) and Water Hyacinth (Eichhornia crassipes)
clogs fish habitat in the African Great Lakes making fishing difficult (Ogutu-Ohwayo et al. 1997).
Wind-pollinated introduced plants can cause allergies and pose a public health concern, as Common
Ragweed (Ambrosia artemisiifolia) has done in Europe (Igrc 1995). Despite decades of active research
(Callaway and Maron 2006), these invasions are likely to increase still more as the developing world
becomes more industrialized; for example, in China, biological invasions are rapidly increasing in
frequency (Ding et al. 2008, Weber and Li 2008).
Despite their negative consequences for the biosphere – indeed, often because of them –
invasions can be tools in our exploration of ecology and evolution (Kolar and Lodge 2001, Lodge
1993, reviewed in Callaway and Maron 2006). To this end they have been studied for a century and a
2
half (Darwin 1859, Elton 2000, Callaway and Maron 2006) and have furthered our understanding of
rapid evolution, community assembly and top-down control of plant populations. Invasion biology has
increased our understanding of population biology (Sakai et al. 2001), the phenomena of rapid
evolution (Blossey and Notzold 1995, Sakai et al. 2001) and the importance of biotic interactions in
determining plant distribution and abundance (Klironomos 2002, Mitchell et al. 2006). Theoretical
approaches to understanding invasions and the communities they invade has progressed from verbal
ideas (Elton 1958) to sophisticated modeling (e.g. Eppstein and Molofsky 2007) taking into account the
multiple interacting factors which together influence invasion.
Much research in Invasion biology is organized around the Enemy Release Hypothesis. The
Enemy Release Hypothesis (ERH) suggests that invaders benefit from a reduced consumer and/or
pathogen load in their new range; it is often invoked to explain the success of non-natives (Elton 1958,
Mitchell et al. 2006, Agrawal and Kotanen 2003, Keane and Crawley 2002, Mitchell and Power 2003,
Maron and Vila 2001, Wolfe 2002). This popular theory has generated a tremendous amount of
discussion and research since it was suggested by Charles Elton 50 years ago and continues to be
refined and explored by modern invasion ecologists (Richardson and Pysek 2008).
Liu and Stiling (2006) identify several assumptions of the ERH, most importantly that top-down
control is important for many plant species and that plants are likely to be introduced without their
oligophagous consumers. Because generalists are present in most habitats and are likely to be able to
feed on invaders (Liu and Stiling 2006, but see Jogesh et al. 2008), invaders continue to experience
some damage in their new habitat. However, because oligophagous consumers in the introduced range
are unlikely to recognize the invader as food, individual plants incur less tissue damage and so enjoy
enhanced probabilities of survival and reproduction. Additionally, invasive plants may be those able to
repel generalist attack as well: for example, in several recent studies (e.g. Jogesh et al. 2008,
3
Cappuccino and Carpenter 2005) exotics were found to be less preferred by native generalists.
Nevertheless the importance of Enemy Release as a cause of invasion is not totally clear;
studies continue to return equivocal results. Colautti et al (2004) found some of this variable evidence
to be linked to the type of study: comparisons of invasives in both their native and exotic range
supported the ERH, while comparisons of exotics and natives within the same community tended to
reject the ERH. In a quantitative review of ERH studies, Liu and Stiling (2006) found support for the
basic assumptions of ERH: introduced populations are attacked by fewer species of insects (in
particular, fewer specialists), and within a community natives receive more damage than invasives. Liu
and Stiling also conclude that studies across the life cycle are necessary to understand how all these
factors together determine plant performance and therefore, invasion success. While whole-lifecycle
studies are increasingly performed, we still have much to learn about the population consequences of
herbivory and its relevance to invasions (Maron and Crone 2006).
The importance of enemy release on the invasiveness of plant populations will depend on many
factors, including the degree of escape from herbivores, the plants’ defensive adaptations and the
habitat in which the herbivore-plant interaction occurs (Mitchell et al. 2006). Below is discussed
variation in the importance of enemies with reference to herbivore natural history, plant life stage when
attacked, the adaptations of plants to herbivory and finally, the abiotic environment wherein these
organisms are interacting.
1.1.1 Type of herbivore damage.
Kotanen and Rosenthal (2000) point out that there are many qualitatively different types of
damage inflicted by invertebrate herbivores, which may be tolerated by different mechanisms and to
different degrees. For example, damage to an apical meristem (i.e. as by some stem galling insects)
can result in the activation of auxiliary meristems, while leaf damage may stimulate an accelerated
Figure 2-2) Germinating seeds from samples of 10 seeds sown on the soil surface
in November 2007 (One-way ANOVA: F2,10 = 0.231, p=0.8,). Seeds were
protected either by a cage (mammal exclusion) or a cage and fungicide (mammal
and fungal exclusion). Control plots were left untouched. Three within-block
replicates were averaged before analysis. Points show means ± 1 SEM (n=6).
44
Control BP BPN
Seedlin
gs s
urv
ivin
g to the e
nd o
f June
02
46
810
Figure 2-3) Seedling survivorship in response to herbivore exclusion treatments.
Points represent the mean, bars the SEM across five blocks. There is an increase
in seedling survivorship with enemy exclusion (Linear contrast in Randomized
block ANOVA: F1,8=6.25, p=0.04,). BP = Barrier and pellets (excluding slugs),
BPN = Barrier, pellets and net (excluding slugs and most insects). Data were log-
transformed in analysis; raw data are shown for clarity.
45
Pro
po
rtio
n o
f le
ave
s d
am
ag
ed
by A
ug
ust
0.0
0.2
0.4
0.6
0.8
1.0
9 plants/m2
25 plants/m2
9 plants/m2
25 plants/m2
Rotenone Water
Disturbed
Undisturbed
Figure 2-4) Damage to adult plants during the summer of 2007. Treatments are
disturbed (cleared plots, filled circles) and undisturbed (uncleared plots, open
circles); high and low density; and insecticide application (Rotenone) and control
(water). Points are means±SEM (n=5). See Table 2-4 for ANOVA results.
46
Pro
po
rtio
n o
f le
ave
s d
am
ag
ed
by A
ug
ust
0.0
0.2
0.4
0.6
0.8
1.0
9 plants/m2
25 plants/m2
9 plants/m2
25 plants/m2
Malathion Water
Disturbed
Undisturbed
Figure 2-5) Damage to individual adult plants during the summer of 2008.
Treatments are disturbed (cleared plots, filled circles) and undisturbed (uncleared
plots, open circles); high and low density; and insecticide application (Malathion)
and control (water). Points are means±SEM (n=5). See Table 2-5 for ANOVA
results.
47
Pro
po
rtio
n o
f p
lan
ts w
ith
ste
m g
alls
0.0
0.2
0.4
0.6
0.8
1.0
9 plants/m2
25 plants/m2
9 plants/m2
25 plants/m2
Malathion Water
Disturbed
Undisturbed
Figure 2-6) The incidence of stem-galling insects on our plants during the summer
of 2008. Treatments are disturbed (cleared plots, filled circles) and undisturbed
(uncleared plots, open circles); high and low density; and pesticide application
(Malathion) and control (water). Points are means±SEM (n=5). See Table 2-7 for
GLMM results.
48
To
tal n
um
be
r o
f le
ave
s
020
40
60
80
100
9 plants/m2
25 plants/m2
9 plants/m2
25 plants/m2
Rotenone Water
A
Ste
m b
iom
ass (
g)
01
23
4
9 plants/m2
25 plants/m2
9 plants/m2
25 plants/m2
Rotenone Water
Disturbed
Undisturbed
BS
urv
ivin
g p
lan
ts
0.0
0.2
0.4
0.6
0.8
1.0
9 plants/m2
25 plants/m2
9 plants/m2
25 plants/m2
Rotenone Water
CT
ota
l n
um
be
r o
f se
ed
s
0200
400
600
800
1200
9 plants/m2
25 plants/m2
9 plants/m2
25 plants/m2
Rotenone Water
D
Figure 2-7) Measures of plant performance in response to a factorial field
experiment in 2007. Treatments are disturbed (cleared plots, filled circles) and
undisturbed (uncleared plots, open circles); high and low density; and pesticide
application (Rotenone) and control (water). Points are means±SEM (n=5). See
Table 2-4 for ANOVA results (Figs A,B and D), and Table 2-6 for GLMM results
(Fig C).
49
To
tal n
um
be
r o
f le
ave
s
20
40
60
80
100
120
9 plants/m2
25 plants/m2
9 plants/m2
25 plants/m2
Malathion Water
A
Ste
m b
iom
ass (
g)
02
46
810
9 plants/m2
25 plants/m2
9 plants/m2
25 plants/m2
Malathion Water
Disturbed
Undisturbed
BS
urv
ivin
g p
lan
ts
0.0
0.2
0.4
0.6
0.8
1.0
9 plants/m2
25 plants/m2
9 plants/m2
25 plants/m2
Malathion Water
CS
ee
d b
iom
ass (
g)
02
46
9 plants/m2
25 plants/m2
9 plants/m2
25 plants/m2
Malathion Water
D
Figure 2-8) Measures of plant performance in response to a factorial field
experiment in 2008. Treatments are disturbed (cleared plots, filled circles) and
undisturbed (uncleared plots, open circles); high and low density; and pesticide
application (Malathion) and control (water). Points are means±SEM (n=5). See
Table 2-5 for ANOVA results (Figs A,B and D), data in Fig C was not analyzed
because almost all plants survived.
50
2.6 Tables
Table 2-1) A table of the common enemies which occur on Ambrosia at KSR. This list was compiled from personal observations and data collected by MacKay and Kotanen (2008)
Taxon Species Damage type Life stage
attacked
Tarachidia
candefacta Hbn.
T. erastrioides Hbn.
(Noctuidae)
Chewing Adult
Zygogramma
suturalis F.
(Chrysomelidae)
Chewing Seedling and
Adult
Beetles
(Coleoptera)
Systena blanda
Melsheimer
(Chrysomelidae)
Chewing Seedling and
Adult
Snails
Trichia striolata
Pfeiffer
(Hygromiidae)
Chewing Seedling
Moth
(Lepidoptera)
Epiblema sp Stem galling Adult
Small
mammals
Seed eating Seed
Table 2-2) ANOVA of enemy exclusion on seed germination. The variation has been partitioned into orthogonal polynomial contrasts to test for an increase in seed survivorship with more complete enemy exclusion. In order, the treatments are: no protection (control), cage (mammal exclusion) or a cage and fungicide (mammal and fungal exclusion). The response variable is mean count of emerged seedlings, natural-log transformed to normalize variance. All terms are tested against the residual with 10 degrees of freedom.
Source df MS F p
Treatment 2 0.025 0.354 0.71 Linear 1 0.031 0.442 0.52
Quadratic 1 0.019 0.265 0.62
Residual 10 0.071
51
Table 2-3) ANOVA of enemy exclusion on seedling survival. The variation has been partitioned into orthogonal polynomial contrasts to test for an increase in seed survivorship with more complete enemy exclusion. In order, the treatments are: no protection (control), BP (aluminum barrier and slug pellets = slug exclusion) or BPN (aluminum barrier, slug pellets and net cover = slug and insect exclusion). Data are natural-log transformed counts of surviving plants. All terms are tested against the residual variance with 8 degrees of freedom.
Source df MS F p
Treatment 2 0.06 3.13 0.1 Linear 1 0.12 6.25 0.04
Quadratic 1 <0.01 <0.01 0.97
Residual 8 0.16
Table 2-4) Factorial ANOVA on the adult experiment in 2007. Leaf number and seed number were log(x+1) transformed before analysis to normalize residuals. F-statistics and p-values are shown in bold typeface when significant.
Leaf Number Stem Biomass Seed Number Damage
Source p F1,28 p F1,28 p F1,28 p F1,28
Density <<0.01 77.19 <0.01 62.51 0.11 2.73 0.28 1.25
Density x Dist. x Spray 0.14 2.31 0.74 0.11 0.30 1.11 0.79 0.07
52
Table 2-5) Factorial ANOVA on the adult experiment in 2008. All values were log-transformed before analysis to normalize residuals, with the exception of damage, which was untransformed. F-statistics and p-values are shown in bold typeface when significant.
Density x Dist. x Spray 0.37 0.84 0.32 1.03 0.47 0.53 0.25 1.36
Table 2-6) Proportion of plants surviving to reproduction in summer 2007, as predicted by all three treatment variables. Likelihood ratio tests were used to simplify a maximal model, which
contained the six parameters shown and additional β for two- and three-way interactions.
Parameter Estimate S.E. z-value P Odds ratio
Fixed effects β0 -0.90 0.18 -4.89 <0.001
βDisturbed 0.87 0.13 6.70 <0.001 2.39 Random effects
Φblock 0.047 0.217
Table 2-7) Proportion of plants attacked by stem-galling insects in 2008, as predicted by all three treatment variables. Likelihood ratio tests were used to simplify a maximal model, only the minimal adequate model is shown.
Parameter Estimate S.E. z-value P Odds ratio
Fixed effects β0 -4.19 1.01 -4.16 <<0.001 0.02
βUndisturbed -2.15 0.53 -4.06 <<0.001 0.12
βwater 3.92 1.03 3.80 <<0.001 50.4
53
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59
3 Leaf damage has weak effects on fecundity in Ambrosia artemisiifolia L.
3.1 Introduction
Throughout the biosphere, plant invasions are becoming increasingly common, presenting
ecologists with both challenges and opportunities. Human activities, particularly habitat alteration and
the intentional and unintentional transport of organisms, have caused rapid, unprecedented mixing of
the Earth’s biota (Elton 1958). Invasive plant species threaten the integrity of both natural and
agricultural systems, and reduce the economic and aesthetic value of land (Vitousek et al. 1997, Mack
et al. 2000). These losses are estimated to total in the billions for Canada’s economy alone (Colautti et
al. 2006); there is great applied interest in understanding invasions so that they can be managed or
prevented (Sakai et al. 2001, Halpern and Underwood 2006). In addition to presenting management
challenges, plant invasions offer an opportunity to learn more about population and community
ecology in general (Kolar and Lodge 2001, Lodge 1993). Studies in invasion biology have contributed
to population biology (Sakai et al. 2001), demonstrated when and to what degree biotic interactions
affect plant distribution and abundance (Klironomos 2002, Mitchell and Power 2003), and informed
management decisions (Colautti et al. 2006).
The Enemy Release Hypothesis (ERH, Elton 1958, reviewed in Keane and Crawley 2002 and
Liu and Stiling 2006), is an important hypothesis within plant invasion biology. The ERH posits that
when plants are introduced to new areas without their ‘enemies’ (i.e. all organisms having direct
negative effects on a plant) the result is increased reproduction and vigour of plants in their introduced
range (Mitchell and Power 2003, Keane and Crawley 2002, Mitchell et al. 2006, Agrawal and Kotanen
2003, Maron and Vila 2001, Wolfe 2002). The importance of invertebrate herbivores in particular has
been emphasized by studies of the ERH (Callaway and Maron 2006).
60
However, population limitation by enemies is not universal: some species possess tolerance
traits that maintain fitness after damage (Kotanen and Rosenthal 2000, Weis and Franks 2006),
buffering the population against top-down control (Tiffin 2000a). Different types of damage are
tolerated in different ways (Tiffin 2000b) which may not necessarily be correlated with one another
(Kotanen and Rosenthal 2000). For example, leaf damage may cause the photosynthetic rates of
remaining tissues to increase (Strauss et al. 2003, Strauss et al. 2002); however, such increases may not
always occur (Caldwell et al 1981) nor may necessarily be a tolerance response (Nowak and Caldwell
1984). On the other hand, damage to the apical meristem, another common mode of plant damage,
often results in rapid regrowth of secondary meristems (reviewed in Tiffin 2000b). Rarely, tolerance
can even take the form of overcompensation, wherein herbivore-attacked plants seem to reproduce
more than their undamaged neighbours (Hawkes and Sullivan 2001). The strength of a species’
tolerance response determines the degree to which it is limited by natural enemies, which in turn
influences how strongly it will respond to enemy release.
To understand how damage relates to fitness, manipulative studies are required; such studies are
most effective in a plant’s native range. Clipping experiments are often useful, because insect attack
rates can vary widely between years (Agrawal and Kotanen 2003), and because estimating tolerance
from natural levels of damage can give a biased estimate (Tiffin and Inouye 2000). Performing such
studies in the native range is important because they allow an assessment of plant responses in a habitat
which contains the biotic and abiotic environment in which it evolved. Because most studies of
invasives are carried out in the exotic range, where they are conspicuous problem species (Colautti et
al. 2004), they may be biased in their measurement of plant response to treatment (Hierro et al. 2005,
Guo 2006). Understanding how – and if – damage to plants causes a reduction of fecundity in their
native range is important to determine how release from damage will contribute to invasion.
61
Ambrosia artemisiifolia (L.) is an ideal system for exploring the relationship between damage
and fitness in an invasive plant. This North American annual is both an agricultural and human health
pest throughout Eurasia, where it spread during the 20th
century (Allard 1943, Chauvel et al. 2006).
Previous studies have confirmed that these plants have indeed experienced escape from enemies during
this invasion: at least in France, individuals are much less attacked than Canadian populations (Genton
et al. 2005). In an attempt to manage ragweed’s invasion, most oligophagous insects which feed on
ragweed have been introduced to Eurasia; however, these attempts have been unsuccessful (Igrc et al.
1995).
We use artificial damage treatments to investigate the relationship between damage and fitness
within a native-range population of ragweed (see Table 3-1). We simulated two damage types,
representing two different groups of enemies: stem borers (“meristem removal”) and leaf chewers
(“leaf clipping”). For each damage type, we asked the following questions: i) does damage decrease
stem biomass (an estimate of plant size) and fecundity (seed mass)? ii) Does damage affect the
relationship between size and fecundity (relative allocation of biomass)?
3.2 Methods
3.2.1 Site
These experiments were conducted at the Koffler Scientific Reserve (KSR) at Joker's Hill, a
350-ha field station owned by the University of Toronto and situated 50km north of Toronto, Ontario
(44 03'N, 79 29'W). A complete plant species list for KSR is provided on the reserve's webpage
(http://www.ksr.utoronto.ca/). Ragweed is common at the site in general and at the experimental site in
particular, emerging readily from the seed bank once our experimental site was cleared. This site
description is also included in Chapter 2, and is included here for completeness.
62
3.2.2 Species
Ragweed is a wind-pollinated spring annual (Bazzaz 1974), germinating late in May and
growing rapidly in open sites. Ragweed is highly disturbance-dependent and is excluded by dense
vegetation (Bazzaz and Mezga 1973, Foster et al. 1980, Stevens and Carson 1999) but grows readily in
weedy, open habitats such as cleared fields (Bazzaz 1974, Kosola and Gross 1999, Maryushkina 1991).
It is difficult to eradicate from a site because of its very long-lived seed bank (Baskin and Baskin
1980). It is widespread throughout its native North America (Bassett and Crompton 1975, Bassett and
Terasmae 1962, Teshler et al. 1981), and its abundant pollen is used by palynologists as an indicator of
human disturbance and agriculture (Grimm et al. 1993). This pollen is highly allergenic and a principle
cause of hayfever (Bassett and Crompton 1975, Bagarozzi and Travis 1998). Ragweed is an important
crop weed and disturbed sites in North America (Bazzaz 1974, Bassett and Crompton 1975) and has
been widely introduced throughout Eurasia, where it has formed successful invasive populations (Kiss
2007).
During invasion, Ambrosia appears to have escaped from its natural enemies: leaf damage is
common in North America but uncommon on populations in France (Genton et al. 2005). Nonetheless,
biocontrol efforts have not been successful, despite the introduction of ragweed-specialized herbivores
such as Zygogramma suturalis (Coleoptera: Chrysomelidae) (Igrc et al. 1995). The insect consumers
from which Ambrosia escaped include both leaf chewing and stem galling herbivores (Table 3-1); we
simulated these damage types in our experimental treatments.
3.2.3 Experimental design
In June 2008, we cleared an experimental plot approximately 30x30m, clearing away old-field
vegetation including a mix of grasses (Bromus, Festuca) and dicots (Cirsium, Asclepias). 150 ragweed
seedlings were gathered from a wild population at KSR and planted in a large cleared field in ten rows
63
(2m apart) of 15 plants, each with 1m between neighbouring plants. Seedlings had 1-2 pairs of mature
leaves and were less than 6cm high at the time of transplanting. Plants were watered for two days
following transplant to protect against transplant shock; plants dying within this period were replaced
(9 plants).
Each row received one of five treatments; two rows were assigned to each treatment
(n=30/treatment). Our five treatments were three levels of leaf removal (75%, 25% and 5%), apical
meristem removal (AM), and an undamaged control (Control). Damage was dispersed evenly over the
entire plant in the 75% and 25% treatments, while in the 5% treatment only fully expanded leaves near
the top of plants were removed in order to make this treatment as repeatable as possible. Leaves were
removed by clipping the petiole close to the stem. Because we removed whole leaves, we delayed
application of the 5% treatment until most plants in this treatment had at least 20 leaves: treatments
were applied to the 75%, 25%, and AM treatments on 16 July 2008 and to the 5% treatment on 28 July
2008. On 26 Aug 2008, all treatments were applied again.
3.2.4 Data collection
In September we collected all surviving plants; at this time growth had ceased and seeds had
matured. After collection, plants were allowed to dry at room temperature before weighing. For each
plant we recorded the mass of all aboveground material (total biomass) and then separated and weighed
the stem and the seeds. We separated seeds from leaf tissue with a 1.4 mm sieve. We used the total
seed biomass as a measure of fecundity, based on the strong relationship between this variable and seed
number (both variables log-transformed, F1,36 = 941.9, r2
= 0.96, p<<0.001).
64
3.2.5 Analyses
i) Are size and reproduction decreased by damage?
We tested for a significant decline in stem biomass or seed production as leaf damage treatment
increases with two separate linear regressions. In this analysis, damage is treated as a continuous
independent variable. We compared the meristem removal treatment to the control in a one-tailed t-
test; meristem removal was hypothesized to reduce growth and reproduction.
ii) Is relative allocation to reproduction decreased by damage?
In contrast to the linear regression described above, our second analysis tests two related
questions: first, does the relationship between plant size and seed biomass change with increasing leaf
damage (i.e. a significant interaction term in the model), and second, if this interaction is significant,
does clipping have a qualitatively different effect for plants of different size? We asked these questions
Figure 3-3) The relationship between seed biomass and plant size (Stem biomass)
changes with response to clipping (F7,109 = 17.59, p<<0.001, r2 = 0.50,). The inset
shows the slopes ± 95% confidence intervals for each line. There is a significant
decline in slope as damage increases (linear contrast = -0.59±0.23, p=0.01); the
75% treatment departs significantly from 1 (grey line).
77
Control 1/20 1/4
Treatments
Ele
vations
0.0
0.2
0.4
0.6
0.8
Figure 3-4) Back-transformed elevations of the lines in Figure 3-3, for each of the
three lowest damage treatments, with 95% confidence intervals. The slopes of
these lines are not different (Figure 3-3), and therefore comparing intercepts
allows a comparison of the different elevations of these lines. Plotting symbols
are the same as in Figure 3-3.
78
1 2 5 10 20
0.0
50.1
00.2
00.5
01.0
02.0
05.0
0
Vegetative biomass (g)
Seed m
ass (
g)
Control
apical
Figure 3-5) The effect of clipping on the relationship between plant size (stem
biomass) and seed mass. Dark lines represent regression lines (±95% CI in lighter
lines). Differences in seed production relative to size are significant (p<0.05)
where the confidence intervals of one line do not include the other. For clarity,
individual data points are omitted.
79
Apical meristem removed Control
−3
−2
−1
01
2
Seed m
ass (
ln(g
))
Figure 3-6) Box-and-whisker plots showing the response of seed mass to apical
meristem clipping. Apical meristem removal does not lower the mass of produced
seeds (one-tailed t-test, t=0.261, p=0.60, df=53.3). Lower and upper edges of
boxes represent the first and third quartile of the data, respectively, while the
upper and lower ‘whiskers’ represent the length of the box multiplied by 1.5.
Notches present an estimate of the value of the median.
80
1 2 5 10 20
0.0
50.1
00.2
00.5
01.0
02.0
05.0
0
Vegetative biomass (g)
Seed m
ass (
g)
apical
Control
control apical
0.0
1.0
2.0
Figure 3-7) Seed production as a function of aboveground biomass for control
and apical-removal treatments. The inset shows slopes ± 95% confidence
intervals. Although the slope is lower for damaged plants, this difference is not
significant (F-ratio: RSSfull = 53.151 with 54 df, RSSreduced = 56.696 with 56 df,
F2,54=1.80, p=0.17)
81
1 2 5 10 20
0.0
50.1
00.2
00.5
01.0
02.0
05.0
0
Vegetative biomass (g)
Seed m
ass (
g)
Control
apical
Figure 3-8) The effect of removing the apical meristem on the relationship
between plant size (vegetative biomass) and seed mass. Dark lines represent
regression lines (±95% CI in lighter lines). Differences in seed production relative
to size are significant (p<0.05) when there is no overlap between CIs. For clarity,
individual data points are omitted.
82
3.8 Tables
Table 3-1) Our damage treatments are intended to replicate the effect of different kinds of damage caused by natural enemies. Here, each experimental treatment is compared to the natural damage it simulates and the insect species which cause that damage. The natural levels of damage are reported from our observations of experimental plants in a separate study, using plants from low-density, cleared, water-sprayed plots (see Chapter 2).
Treatment Damage Type Insect species Natural levels (from
Chapter 2, 2008 data)
Zygogramma suturalis F.
(Coleoptera: Chrysomelidae)
Systena blanda Melshimer
(Coleoptera: Chrysomelidae)
Corythucha spp.
(Heteroptera: Tingidae)
Leaf clipping
Chewing
Tarachidia spp.
(Lepidoptera: Noctuidae)
Leaves damaged:
52.4%
Meristem
removal
Stem galling Epiblema sp. Stems galled:
0.62 (±0.32) %
83
Table 3-2) ANOVA table for the linear model including plant size (stem biomass) as a continuous variable and clipping as an ordered factor. Sums of squares are partitioned into orthogonal polynomials to test the a priori hypothesis that clipping lowers reproduction relative to plant size. All three contrasts (Linear, quadratic and cubic) are shown; higher order terms are not significant. All terms are tested against the residual.
Source df MS F P
Ln(stem biomass) 1 84.45 98.3 <0.001
Damage 3 3.84 4.47 0.005
Linear 1 10.32 12.00 <0.001
Quadratic 1 0.02 0.02 0.89
Cubic 1 1.19 1.38 0.24
Ln(stem biomass)*Damage 3 3.29 3.83 0.012
Linear 1 8.08 9.39 0.003
Quadratic 1 1.72 2.01 0.16
Cubic 1 0.07 0.08 0.78
Residual 109 0.86
Table 3-3)Parameter estimates (SE) for slopes and intercepts from the linear model of log(seed mass) on log(stem mass).
Level of Intercept Slope
Control -1.93 (0.38) 1.24 (0.26) 5% -1.77 (0.26) 1.23 (0.16)
25% -1.00 (0.32) 1.04 (0.20)
75% -0.45 (0.22) 0.43 (0.19)
84
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4 General Discussion
A reduced herbivore load following introduction is predicted to increase demographic success
of introduced plants, as predicted by the Enemy Release Hypothesis (ERH). However, studies of the
Enemy Release Hypothesis are predicated on the assumption that strong consumer effects are present at
some stage in the life cycle. In this thesis I present the results of experiments investigating the effects
of enemies on all life stages in Ambrosia artemisiifolia. This work asks two complementary questions:
first, how does enemy exclusion affect plant performance across three life history categories: seed,
seedling and adult? Second, how does leaf damage change the relationship between plant growth and
seed production in this species?
This general discussion has three parts: first, a summary of my experimental results. Second, a
discussion of their relevance to the natural history of Ambrosia in Canada, its invasion of Eurasia, and
biological invasions in general. Finally, a suggestion of interesting future research questions, including
the presentation of some suggestive ancillary results from the present study.
4.1 Summary of results The effects of enemy exclusion were in general weak in this species, as reported in Chapter 2. I
was not able to find evidence of strong enemy effects at the seed stage, while at the seedling stage such
effects were present but weak. Our pesticide spray successfully prevented insect damage and was more
effective in 2008;however in neither year did plants experience an increase in performance relative to
water controls.
Disturbance, in contrast, had a very large impact on ragweed performance. Adult plants in
disturbed areas survived better during the dry summer of 2007. The following year, though nearly all
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plants survived, plants in disturbed plots showed greatly increased growth and reproduction relative to
plants growing among old-field vegetation.
In the tolerance experiment (Chapter 3), I found that leaf damage had no direct effects on seed
production and depressed growth very little. However, allocation to reproduction relative to stem
biomass was increased by leaf damage. This same analysis produced evidence of a small effect of
overcompensation in plants which experience light (25%) damage.
4.2 Ambrosia and invasions
4.2.1 Ragweed in North America
Disturbance is the primary influence on the population size and density of ragweed plants
(Teshler 1981, Stevens and Carson 1999). A native weed of disturbed ground in contemporary Canada,
ragweed is considered a crop weed (Bassett and Crompton 1975), a nuisance plant, and an important
source of allergenic pollen (Bagarozzi and Travis 1998). Clues to the pre-historical distribution of
ragweed are found in pollen records, which show that ragweed plants have historically lived on
disturbed sites (Grimm 1993). Lake pollen records show great fluctuation in the amount of “Ambrosia-
type” pollen throughout the Holocene, possibly in relation to disturbance caused by drought (Grimm
2001).
As European agriculture was transferred to North America, the rapid and heavy disturbance
created ideal ragweed habitat. Disturbed sites also favour the survival of seeds, as rodents do not
frequently go into open areas where they risk predation from birds (Manson and Stiles 1998). In
addition, ragweed plants have long-lived seeds (Baskin and Baskin 1980) – a common trait among
disturbance-adapted plants (Baker 1965). Seeds are not rapidly consumed by mammals and fungi,
which likely helps their seed banks build up to large sizes in cropland.
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4.2.2 Ragweed’s Invasions
Because Ambrosia is so dependent on disturbance, it is not surprising that it is most invasive in
disturbed and agricultural land in the introduced range (Chauvel et al. 2006). However, Ambrosia is
also extremely herbivore-tolerant, which may make biological control challenging. Biocontrol agents,
such as Z. suturalis, have not been successful in Eurasia. This could be because populations have not
always established well there (Igrc 1995). However, even if large, stable populations do establish,
control efforts may prove difficult because ragweed is very tolerant to leaf damage. A successful
biocontrol agent would have to remove a great deal of leaf tissue, more than the 75% of tissue we
removed in our experiment, to reduce fecundity in ragweed.
This high level of tolerance also explains the absence of any evolutionary change in ragweed
following introduction (Genton et al. 2005): if enemies do not exert selection in the native range, then
their absence will not create a change in selection pressures in the introduced range (Franks et al.
2008).
4.2.3 Invasions in general
Disturbed sites have more invaders (Mack et al. 2000), and plants specifically adapted to
disturbance in the native range may be particularly likely to become invaders (Cadotte 2006). As well,
because disturbance creates open ground not dominated by the resident community, it can provide a
release from the ‘biotic resistance’ that introduced plants may face in their new range (Maron and Vila
2001).
The effects of disturbance can exaggerate the positive effects of enemy release (Blumenthal
2005, 2006). Blumenthal suggests that enemy release has a far greater effect when the introduced
species are adapted to rapidly use available resources. Ragweed, like many weeds of disturbed ground,
is adapted to disturbed ground with abundant resources. Our experiment could have detected this
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synergistic effect as an interaction between disturbance and pesticide application, but no such
interaction was observed. However, it is possible that in Eurasia, ragweed is even less damaged, or that
European sites are richer in nutrients, thereby increasing the effect of enemy release to a biologically
meaningful level.
Generally, the ERH is predicated on the assumption that enemies matter. Indeed, studies of the
ERH often test hypothesis about the distribution of leaf damage, without demonstrating a fitness cost
(Maron and Vila 2001). As studies of invaders in the native and introduced ranges accumulate,
ecologists will develop a better idea of the relationship between enemy attack and population dynamics
for invasive plants. I suggest that the importance of the enemy release hypothesis has been over-
estimated.
4.3 Suggestions for future work I consider Annual Ragweed a excellent and tractable study system, which could be used in
future to continue the pattern in invasion biology of simultaneously investigating biological invasions
per se and basic ecology. There are many interesting questions remaining both within this system and
in invasion biology in general. Because each experiment I conducted raised distinct questions, this
section is again structured by experiment.
4.3.1 Seeds
Ragweed achenes have very hard coats that can not be broken easily once the seeds are mature.
Therefore, important seed predation may not occur after dispersal – rather the predispersal predation
stage may be more important. In particular, (MacKay and Kotanen 2008) found Harpalus rufipes
eating seeds before they are dropped from the plant -- interestingly, this is a European species. Eurosta
bellis was also observed consuming seeds pre-dispersal, leaving characteristic holes punched in the
seed coat. I performed some small preliminary “no-choice” trials, both with Carabids and Field
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Crickets (Orthoptera: Gryllidae), by enclosing a sample of seeds with an insect and checking regularly.
I found it very difficult to observe Carabid predation in these artificial conditions: most of these beetles
starved, unable to break the seed coat. Crickets, on the other hand, are able to eat at least some seeds in
captivity, perhaps due to their larger size. It would be interesting to extend these trials by sampling
common omnivorous invertebrates from KSR over a summer and testing their ability to feed on the
seeds of several old-field species, including ragweed. This could establish whether ragweed is an
exceptionally tough-seeded plant, or if such durable seeds are common. Even more interesting would
be a repetition of the same study in France as well, testing the hypotheses that tougher seeds have
allowed ragweed to invade.
4.3.2 Seedlings
Ragweed plants are quite late-germinating; they may be among the last annual plants to emerge
in the spring. However, they are nevertheless often very conspicuous by the end of the summer and
have been considered ‘successional dominants’ (Bazzaz 1974, Bassett and Crompton 1975) in the early
stages of old field succession. Why is seedling germination so late? One possibility is that seedling
predation is much greater earlier in the season – this could be tested by planting out young ragweed
seedlings each week from early May to late June, and observing survival. Perhaps the phenology of
Ambrosia relative to the Eurasian flora further increases its enemy release there, avoiding important
seedling predators that might reduce populations of competitors earlier in the season.
4.3.3 Mechanisms of tolerance and allocation
The high level of tolerance in Ambrosia makes it a good system for asking questions about
mechanisms and evolution of tolerance. More detailed studies which examine the plant responses in
detail (measuring the branching pattern, photosynthetic rate, etc) are needed to unambiguously
investigate the mechanism of tolerance in a species. For example, Huhta et al. (2000), also investigated
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several levels of clipping damage, crossing this treatment with fertilizer and competition treatments. In
addition to measuring reproduction they quantified plant architecture to test the hypothesis that release
from apical dominance was the mechanism of tolerance in this species.
I quantified seed production (female function) in my tolerance study (Chapter 3), however,
pollen dispersal (male function) is another important means of reproduction. The degrees of tolerance
to herbivory may be different between female and male function. For example, Strauss et al. (2003)
found that male and female tolerance in Raphanus raphanistrum were not correlated, although male
fitness was less variable. While measuring seed production alone is useful for predicting population
growth, measuring pollen production is also important. In particular, an important aspect of ragweed’s
impact as a weed (in Canada) and an invader (in Europe) is its production of large amounts of
windborne, highly allergenic pollen (Bagarozzi and Travis 1998). Therefore, a study which examines
herbivory on plants and pollen production would have both basic and applied significance.
In addition, I would suggest a future study to examine another possible sex-allocation response
to herbivory: plants may be using herbivory as an indicator of conspecific density. Such phenotypic
‘adjustment’ of sex ratio on the part of a growing plant has been recently demonstrated: many plant
species are capable of modifying their growth pattern when exposed to red/far red ratios indicative of
crowded conditions (Schmitt et al. 2003). Herbivores could act in a similar way as indicators, not
merely of the presence of nearby plants (as the red/far red ratio does), but of conspecific density in
particular. This would be the case if two conditions held: if the majority of damage is caused by
oligophagous or specialist consumers (as opposed to broad generalists), and if these attack plants in a
density-dependent fashion (i.e. as suggested by the Janzen-Connell mechanism, Janzen 1970, Connell
1971). This pattern of decline in attack with increasing distance from conspecifics has been
demonstrated for many tropical species (Hyatt et al. 2003) and recently for Ambrosia itself (MacKay
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and Kotanen 2008).
Wind pollinated plants are sometimes pollen-limited, as has been demonstrated in another
anemophilous invasive, Spartina alterniflora (Davis et al. 2004). In fact, isolated Ambrosia plants set
less seed than plants in dense populations; ragweed plants are self-incompatible (Friedman and
Barrett). If pollen limitation were a problem for ragweed, then isolated individuals may be able to
increase fitness by producing more male flowers, as female flowers are likely to remain un-pollinated.
Conversely, plants near to conspecifics would not be pollen-limited. If the amount of herbivore damage
is a reliable signal of conspecific density, this may provide useful ‘cues’ to plants. Such plasticity in
within-plant sex ratios is well-documented in this species: the within-plant sex ratio of Ambrosia
becomes increasingly female under light limitation, and increasingly male under nutrient limitation
(Paquin and Aarssen 2004).
While my experiments were not designed to test these hypotheses, a rough estimate is still
possible. By weighing the clipped leaves from all plants (see Chapter 3) we were able to estimate the
relationship between leaf number and leaf mass. Then, the mass of all male flowers can be determined
by:
Male flowers = total biomass – stem(g) – seed(g) – predicted leaves (g)
where leaf mass is predicted using a count of leaves at the end of August. Changes in the
relative allocation of biomass to male vs. female function can then be investigated with an ANCOVA-
style plot (as was used in Chapter 3). The results are shown in Figure 1.
Examining the slope values in this relationship (inset) shows that ragweed produces more seed
biomass than flower biomass, and that this relationship increases with clipping damage. This pattern is
consistent with the ‘cheap pollen’ but not with my suggested mechanism and is consistent with the
98
results of (Strauss et al. 2003). However, this approach is only a rough estimate and, in particular, the
comparison is more appropriate between the mass of female flowers and male flowers. Nevertheless,
this data highlights the need to consider both male and female function when assessing reproductive
output.
4.3.4 Indirect effects of tolerance
It is possible that introduced species, when they reach high population sizes in their new range,
are able to exert indirect interactions on the community and so increase their invasiveness. It has been
suggested (Ghazoul 2002) that species which have very large floral displays are over-attractive to
pollinators, and so reduce the reproduction of native plants. Similar interactions are possible for very
tolerant species. If a plant is very tolerant, it suffers less limitations of its population growth as a result
of consumer pressure. However, herbivores of tolerant plants may spill over to neighbours. Thus,
tolerance adaptations may confer an advantage on an invading plant not only by magnifying the effect
of enemy release, but also by increasing the amount of top-down control on neighbouring plants.
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0.01 0.05 0.50 5.00
5e−
03
5e−
02
5e−
01
5e+
00
Mass of seeds produced (g)
Estim
ate
d m
ale
flo
wer
mass (
g)
Control
5%
25%
75%
Control 1/20 1/4 3/4
Slo
pe
0.0
0.5
1.0
1.5
2.0
Figure 4-1) A rough estimate of male flower mass compared to the mass of seeds
produced for each plant in the Tolerance experiment (details in Chapter 3). The
allocation to male function over female function increases with increasing damage
(inset).
100
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