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dissertation entitled

THE ECOLOGY OF THE EXOTIC, INVASlVE TEMPERATE
LIANA CELASTRUS ORBICULATUS (ORIENTAL BITTERSWEET)

presented by

Timothy Jay Tibbetts

has been accepted towards fulfillment
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Ph.D. , Botany and Plant Pathology
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6/01 cJCIRC/DateDuepss-p. 1 5

THE ECOLOGY OF THE EXOTIC, INVASIVE TEMPERATE LIANA CELASTRUS
ORBICULATUS (ORIENTAL BITTERSWEET)

BY

Timothy Jay Tibbetts

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

DOCTOR OF PHILOSOPHY

Department of Botany and Plant Pathology

2000

ABSTRACT

THE ECOLOGY OF THE EXOTIC, INVASIVE TEMPERATE LIANA CELASTRUS
' ORBICULATUS (ORIENTAL BITTERSWEET)

By

Timothy Jay Tibbetts

The exotic liana (woody vine) Celastrus orbiculatus was
compared to co-occurring plants of the native species C.
scandens and Vitis riparia in south central Michigan. The
successful invasion of C. orbiculatus does not appear to be
related to hydraulic advantages over native lianas. Cblastrus
orbiculatus lacks the root pressure mechanism.seen in V;
riparia and lacks any advantage in hydraulic conductance.
These findings indicate that root pressure is not a requisite
characteristic for success as a temperate liana.

Reproductive characters observed in C. orbiculatus
indicate a clear advantage over the native congener C.
scandens. CElastrus orbiculatus produces more seeds that are
smaller and have a greater chance of germinating than seeds
of C. scandéns. These trends hold true across several sites,
and over two years.

Shoot elongation measurements of C. orbiculatus and V.
riparia over two years failed to demonstrate differences in
maximum.shoot length. In one year, C. orbiculatus enjoyed a

longer growing season by maturing earlier and retaining

leaves longer than V: riparia. Incidence of herbivory was
similar in these species, however, V1 riparia shoots suffered
a higher rate of mortality.

Dendrochronology proves to be a useful tool in the
investigation of liana invasion. Both C. orbiculatus and V.
riparia demonstrate sensitivity in annual ring widths that is
reproducible within individuals and between individuals at
the same site. The chronologies developed indicate that
Kellogg Biological Station was invaded.by C. orbiculatus at
least by 1952, Hidden Lake Gardens by 1971, and the Petrides
farm by 1972.

Celastrus orbiculatus appears to thrive in Michigan for
numerous reasons: reduced effects of herbivory and
competitors in the form of other plant species using the same
niches. The frequent and large scale disturbances
characteristic of many temperate ecosystems also enhance the
opportunities for exotic species such as C. orbiculatus to

establish, persist, and invade.

ACKNOWLEDGEMENTS

I thank my advisor and friend, Dr. Frank Ewers, for
allowing me to find my own way into this wonderful project.
Without considerable understanding on his part, I would never
have had the great graduate school experience I have managed.

I additionally thank the other members of my graduate
committee: Dr. Peter Murphy, Dr. Frank Telewski, and Dr. Jim
Flore. Their guidance has been vital.

Grateful appreciation is expressed to Frank Telewski,
Jack Wolf, Ellyn Meyers, George Petrides, and Bob Herner for
use of sites.

NUmerous MSU undergraduate students participated in
various parts of this research. Aimee Pumarejo and Jen Busser
were indispensable in some of the hydraulic conductivity and
root pressure studies.

Fellow graduate students past and present have served as
sources of inspiration, guides, and mentors. No list could
ever be complete.

My wife Amy has supported me and this work and suffered
through the trials and tribulations. I owe her everything.

My parents have been the staunchest supporters,
encouraging me along the way, and avoiding asking the “when"

question every graduate student parent is tempted to ask.

iv

TABLE OF CONTENTS

LIST OF TABLES ..............................................

LIST OF FIGURES .............................................

CHAPTER 1
EXOTIC LIANAS IN TEMPERATE ECOSYSTEMS: INVADABLE COMMUNITIES
OR EFFECTIVE INVADERS?

Introduction ........................................... 1
Communities and Disturbance ............................ 2
Invasion ecology ....................................... 5

Characteristics of exotic lianas leading to invasion...7
Case Studies: Community invasions by exotic lianas....ll
Conclusions ........................................... 14

CHAPTER 2
CELASTRUS ORBICULATUS (ORIENTAL BITTERSWEET) NATURAL HISTORY
AND PRESENCE IN MICHIGAN

Introduction .......................................... 15
Taxonomy .............................................. 15
Distribution of the genus ............................. 17
Biology ............................................... 18
Ecology in native range ............................... 19
Introduction to NOrth America ......................... 21
Status in Michigan .................................... 22
Species used in this research ......................... 23

CHAPTER 3

ROOT PRESSURE AND SPECIFIC CONDUCTIVITY IN TEMPERATE LIANAS:
EXOTIC CELASTRUS ORBICULATUS (CELASTRACEAE) VS. NATIVE VITIS
RIPARIA (VITACEAE)

Introduction .......................................... 29
Methods and materials ................................. 33
Results ............................................... 38
Discussion ............................................ 50

CHAPTER 4
SEED PRODUCTION AND GERMINATION IN THE INVASIVE LIANA
CELASTRUS ORBICULATUS AND THE NATIVE C. SCANDENS

Introduction .......................................... 56
Methods and materials ................................. 58
Results and discussion ................................ 6O

CHAPTER 5
GROWTH, PHENOLOGY, AND HERBIVORY IN CELASTRUS ORBICULATUS AND
VITIS RIPARIA

Introduction .......................................... 72

Methods and materials ................................. 74

Results ............................................... 76

Discussion ............................................ 80
CHAPTER 6

DENDROCHRONOLOGY APPLIED TO THE EXOTIC TEMPERATE LIANAS
CELASTRUS ORBICULATUS AND NATIVE VITIS RIPARIA

Introduction .......................................... 85
Methods and materials ................................. 86
Results ............................................... 89
Discussion ........................................... 104
CHAPTER 7
GENERAL
CONCLUSIONS ............................................... 108
BIBLIOGRAPHY .............................................. 114

vi

LIST OF TABLES

Table 3-1. Site descriptions. Names. locations, and
descriptions of the forest types and soils present,
in each of the study sites in Michigan ..................... 34

Table 4-1. Seed germination trial conditions ............... 61

Table 5-1. Phenology. Julian date 1 1 SE. An asterisk

below a column indicates a significant difference

between the species in a two—tailed t-test at alpha =

0.05 ....................................................... 77

Table 5-2. Herbivory and Mortality. Percentage;t 1 SE.

An asterisk below a column indicates a significant
difference between the species in a two-tailed t-test

at alpha = 0.05 ............................................ 77

Table 6-1. Dendrochronology site locations (Michigan) ...... 88
Table 6-2. Correlation analysis of precipitation and

ring width. Summer precipitation = June + July + August
precipitation ............................................. 100

vii

LIST OF FIGURES

Figure 2-1. celastrus orbiculatus distribution, 1985
(after Voss 1985) .......................................... 25

Figure 2—2. Cblastrus orbiculatus distribution, 2000 ....... 26

Figure 2-3. Cblastrus scandens distribution, (after
Voss 1985) ................................................. 27

Figure 2—4. Vitis riparia distribution, (after Voss
1985) ...................................................... 28

Figure 3—1. Root pressure. (A) 1996. (B) 1997. Each

symbol represents the mean for five stems. The range

for V3 riparia is 0-145 kPa. Error bars represent 1

1 SE. Where error bars are not visible, they are

smaller than the plotted symbol. Relative phenological
events are indicated by arrows (white arrows = V.

riparia and black arrows = C. orbiculatus) ................. 39

Figure 3-2. Percentage embolism” (A) 1996. (B) 1997.

Each symbol represents the mean for five stems. Error

bars represent 1 1 SE. Where error bars are not visible,

they are smaller than the plotted symbol. Relative
phenological events are indicated by arrows (white

arrows = V: riparia and black arrows = C. orbiculatus).

Some relevant minimum.daily temperatures are indicated

along the top .............................................. 41

Figure 3—3. Initial (native) specific conductivity

(ks). (A) 1996. (B) 1997. Each symbol represents the

mean for five stems. Error bars represent 1 1 SE.

Where error bars are not visible, they are smaller

than the plotted symbol .................................... 43

Figure 3-4. Final (maximum) specific conductivity

(k3). (A) 1996. (B) 1997. Each symbol represents the

mean for five stems. Error bars represent 1 1 SE.

Where error bars are not visible, they are smaller

than the plotted symbol .................................... 44

viii

Figure 3—5. Number of active (conductive) growth

rings. Error bars represent 1 1 SE. Where error

bars are not visible, they are smaller than the

plotted symbol ............................................. 46

Figures 3-6 to 3-13. Transverse view of stems. Scale
bar = 200 um.and applies to all figures. Perfusion
of stems with crystal-violet marked conductive
vessels. Stems were collected from the same site on
two different dates. Figures 3-6 to 3—9. Stems
collected on 30 April 1997. 3-6. Celastrus
orbiculatus, native state. The arrows indicate
conductive vessels. 3-7. Vitis riparia, native

state. 3-8. C. orbiculatus, after being flushed to
remove embolism- 3-9. V: riparia, flushed. Figures
3-10 to 3-13. Stems collected on 18 June 1997. 3-10.
C. orbiculatus, native state. The white arrow
indicates a conductive growth ring; the black arrow
indicates a nonconductive growth ring. 3-11. V.
riparia, native state. 3-12. C. orbiculatus, flushed.
The white arrows indicate conductive growth rings.
3-13. V: riparia, flushed .................................. 48

Figure 3-14. Frequency distributions of vessel

diameters (histograms) and percentage of total

theoretical kh (filled circles). (A) V: riparia.

(B) C. orbiculatus. Based upon vessels from.stems

shown in figures 3—6, 3-7, 3—10, and 3-11 .................. 49

Figure 3—15. vulnerability curves. Each symbol

represents the mean for five stems. Error bars

represent 1 1 SE. Where error bars are not visible,

they are smaller than the plotted symbol ................... 51

Figure 4—1. Mean seeds per fruit, 1 1 SE. Sample

sizes are as follows: C. scandens at MSU N = 193,

Rose Lake N = 57, Shoeman Road N = 140; C.

orbiculatus at MSU N = 312, K38 N = 336, Hidden

Lake Gardens N = 355. Bars designated with different

letters are significantly different from one another

with P < 0.05 .............................................. 62

ix

Figure 4-2. Mass per seed. Sample sizes are as
follows: C. scandens at MSU'N = 453, Rose Lake

N = 234, Shoeman Road N = 376; C. orbiculatus at
MSU N = 921, KBS N = 236, Williamston N = 624.
Seeds were weighed en masse, so SE could not be
calculated ........................................

Figure 4-3. Germination trials. Open symbols for
C. scandens, closed symbols for C. orbiculatus.
See Table 4—1 for the conditions of each separate
trial .............................................

Figure 5-1. Mean shoot length, i 1 SE. (A) 1998.
(B) 1999. Low light level < 1000 lux, high light
level > 1000 lux ..................................

Figure 5—2. Sources of mortality, 1998 and 1999.
NOte that the total mortality was greater in V;
riparia both years (see Table 5-2) ................

Figure 5-3. Precipitation. (A) 1998. (B) 1999.
Monthly totals from.the Kellogg Biological Station
Long Term Ecological Research site weather station

Figure 5-4. Temperature. (A) 1998. (B) 1999. Mean
monthly temperature from the Kellogg Biological

Station Long Term Ecological Research site weather
station ...........................................

Figure 6—1. (A) Annual precipitation at Petrides
farm” (B) C. orbiculatus ring width chronology.
The separate lines represent two chronologies for
the same individual ...............................

Figure 6-2. (A) Annual precipitation at Kellogg
Biological Station. (B) C. orbiculatus ring width
chronology. The separate lines represent two
chronologies for the same individual ..............

......... 65

......... 67

......... 78

......... 80

......... 81

......... 82

......... 90

......... 91

Figure 6—3. (A) Annual precipitation at Kellogg

Biological Station. (B) V: riparia ring width

chronology. The separate lines represent two

chronologies for the same individual ....................... 92

Figure 6-4. Ring width chronologies for C.

orbiculatus at KBS. Each plot represents the

mean ring width for one individual. NOte the

consistent valley at 1979 .................................. 94

Figure 6—5. Ring width chronologies for V.

riparia at KBS. Each plot represents the

mean ring width for one individual. Note the

consistent valley at 1974 .................................. 95

Figure 6—6. A. Annual precipitation at Petrides
farm” B. Mean ring width of C. orbiculatus, +/- 1 SE ....... 96

Figure 6-7. A. Annual precipitation at Kellogg
Biological Station. B. Mean ring width, +/- 1 SE ........... 97

Figure 6-8. A. Annual precipitation at Hidden
Lake Gardens. B. Ring width, +/- 1 SE ...................... 98

Figure 6-9. Lifespan of vines sampled at Petrides
farm” Each horizontal line represents one individual ...... 101

Figure 6-10. Lifespan of vines sampled at Hidden
lake Gardens. Each horizontal line represents one
individual ................................................ 102

Figure 6-11. Lifespan of vines sampled at Kellogg
Biological Station. Each horizontal line represents
one individual ............................................ 103

xi

CW1
Exotic lianas in temperate ecosystems: invedeble communities

or effective invaders?

Introduction

Vines occur across taxonomic divisions, in ferns,
gymnosperms and angiosperms. Climbers occur in monocots as
well as dicots and in 133 plant families, indicating that the
adaptation for a climbing habit has evolved numerous times
(Gentry 1991). However, the distribution of lianas (woody
vines) across the globe is disproportionate. Lianas are
generally more prevalent in tropical ecosystems (19% of
floras) than in temperate ecosystems (6% of floras) (Gentry
1991). In Michigan, lianas comprise only about 1% of the
flora (29 species of 2465 total as reported in Voss, 1972,
1985, 1996). The relative rarity of the climbing growth form
in the temperate landscape indicates that there may be
factors that limit their distribution, probably low
temperatures and limited moisture (Ewers 1985, Sperry and
Sullivan 1992, Hargrave et a1. 1994).

Although lianas are generally minor components of
temperate forest communities, there are some notable
exceptions in eastern North America: Pueraria lobata
Willd.(kudzu), Lonicera japonica Thunb. (Japanese

honeysuckle), Celastrus orbiculatus Thunb. (Oriental

bittersweet), Passiflora mollissima, and Rosa (multiflora
Wechsler 1977, Patterson 1974, Slezak 1976). These introduced
lianas have become temperate zone “weeds" displacing native
species and are capable of changing community dynamics
(Penfound 1966) and damaging native species (Trimble and
Tryon 1974, Lutz 1943). In light of these temperate weedy
lianas, we can explore two hypotheses that are not mutually
exclusive: 1) some temperate plant communities are
particularly prone to invasion, and 2) some exotic lianas are

preadapted or predisposed to becoming successful invaders.

Communities and Disturbance

The harsh NOrth American climate and poor liana habitat
may help explain the paucity of temperate lianas relative to
both temperate South America and temperate Asia, which have
greater liana diversity (Gentry 1991).However, this low liana
diversity and abundance also indicates that the liana niche
is largely open in North American plant communities. Given
the low potential for competition with native lianas,
invading lianas may have the potential for explosive spread.

Disturbance and its effects on ecosystem function
frequently favors invasion (Orians 1986). Successful invasion
may only be possible if it coincides with disturbance.
Crawley (1986) looked for pattern to explain Britain’s alien

plant problem. It is estimated that ten times more plant

species have been introduced to the British Isles than are
recognized as members of the “native" flora. Crawley (1986)
found that successful establishment of an alien plant species
depended on disturbance of the soil surface and the amount of
exposed bare ground due to low plant cover in a given
community. Secondary factors included proximity to sources of
alien propagules and the rate of propagule dispersal.
Clearly, since natural disturbances are stochastic, any
community is potentially invadable (Crawley 1986).

Temperate forest communities are subject to natural
disturbances including catastrophic wind-throw, tornadoes,
downbursts accompanying thunderstorms, ice storms, fires,
herbivory, and disease epidemics (Davis 1987). More mature
stages of succession may suffer less frequent disturbance;
their advanced stage is evidence of a long time period
without disturbance (Robertson et a1. 1996). However, the
chance of disturbance still remains, and directly following
disturbance the presence of bare ground can act as a catalyst
for invasion. Indeed, one interpretation of the process of
succession is the repeated invasion by new species.

Davis (1987) looked at the invasion of temperate forest
communities using pollen records. Disturbance was responsible
for opening the canopy, however secondary factors were
important in determining the success of invasion. The

presence of invaders in the successional communities depended

on whether they were already present in the seed bank or as

juveniles. Thus the timing of invading species introduction

through dispersal is critical. Young, even-aged successional
stands, more common following large disturbance, offered.few
gaps for invasion (Davis 1987).

Human disturbance of communities is not stochastic.
Forestry practices such as logging create open space
available for invasion. Wildlife management practices often
intentionally create and maintain “edge" habitat using
disturbance. In addition, humans increase the distribution
and dispersal of alien propagules, either intentionally or
unintentionally (Crawley 1987). The purposeful introduction
of exotic species for wildlife use (food, cover) or
ecological purposes (erosion control) can have undesired
results. Human activities also continually reduce the size of
natural areas and decrease the isolation of sites through
road building and settlement. These practices can open space
for invasion and lead to the establishment of exotic species.

Without detailed information on all the resource levels
in a community and the requirements of the species present,
predicting whether a community is likely to be invaded can be
based only on plant cover as a surrogate and the local
disturbance regime. This implies that communities are
universally invadable. It will be useful to look at the

attributes of species that make them effective invaders.

Models based on these characteristics may be helpful for

predicting invasion.

Invasion ecology

Invading species are frequently considered weeds. A
weed is subjectively defined as a plant growing where it is
not desired. Weeds can be native or exotic species under this
definition. Life-history patterns have been divided into r—
and Keselected, with r-selected species maximizing
reproduction by producing many, small young that mature
rapidly and require little care while Keselected species
target carrying capacity and produce fewer, larger young that
mature slower and receive intensive care (MacArthur & Wilson
1967, Pianka 1970). This scheme is clearly an
oversimplification, and any species will demonstrate traits
of both strategies. However, in general one would expect
weeds to be relatively r-selected, having rapid development,
short life span, semalparity, small body size, and many small
seeds (MacArthur & Wilson 1967, Pianka 1970).

Grime (1979) refined the r- Selected pattern and defined
weeds (ruderals) as being small herbs with short life spans,
devoting most of their production into many seeds, having
high potential relative growth rate, and having varied but
often high palatability to herbivores. A number of these

traits are found in exotic lianas.

Rejmanek and Richardson (1996) attempted to identify the
characteristics of pines that explained why some species
became successful invaders while others did not. They found
that low seed mass, high frequency of large seed crops, and
short time spent as a juvenile were traits found in the weedy
pine species. These traits follow Grime's (1979) ruderal
classification. Rejmanek and Richardson (1996) then showed
that a discriminant function based on these characteristics
was highly effective for correctly identifying non—pine
species as invasive or non-invasive (38 of 40 species). This
analysis included numerous weedy vines problematic in Nerth
America (Lonicera japonica, Pueraria lobata, Passiflora
.mollissima, and Rosa.mu1tiflora). It appears that life
history characters can successfully be applied to predict
weediness and invasive ability (Rejmének & Richardson, 1996).

The frequency at which exotic species become weeds has
been generalized in the “tens rule" of Williamson and Fitter
(1996). For simplification, the invasion process can be
broken into stages: arrival, establishment, and integration
(vermeij 1996). In short, one in ten of those species
“imported" will appear in the wild, one in ten of those
appearing in the wild will become established, and one in ten
of those established will become a pest. This means that 1 in
1000 species introduced will have a negative economic effect

as a pest. The tens rule is a generalization that works for a

large number of organism groups (Williamson & Fitter 1996).
Possible reasons for exotic species to succeed as weeds are
the lack of their native pests, diseases, and competitors. At
the same time, a lack of pollinators and dispersal agents can
be problematic for exotic plant species (Crawley 1987). The
rule of tens demonstrates that most species introductions
fail.

Characteristics of exotic lianas leading to invasion

The defining characteristics of vines may indicate why
they can potentially be weeds. They are “mechanical
parasites,” meaning they depend on external support for
vertical growth (Stevens 1987). A liana is a woody vine with
secondary growth. The liana stem.is characteristically
narrow, with long and.wide vessels, providing lots of
conductive vessel area, and often has anomalous secondary
growth patterns, making for flexible stems. There is often a
high ratio of leaf to stem area. These characters combine to
make lianas highly effective at water transport with a
minimal investment in structural support (Ewers et al. 1991,
Fisher & Ewers 1991).

Lianas native to North America, e.g., Parthenocissus,
Vitis, and Tbxicodendron, are capable of reaching the tops of
tall trees and shading out their hosts. These vines rarely
develop into thick monospecific stands to the exclusion of

other species (except see Trimble & Tryon 1974, Siccama et

a1. 1976). However, three exotic lianas are particular
problems in North America: Pueraria lobata (kudzu), celastrus
orbiculatus (oriental bittersweet) and Lonicera japonica
(Japanese honeysuckle)(Wechsler 1977, Patterson 1974, Slezak
1976). Comparisons of C. orbiculatus and L. japonica with
their far less prevalent native sympatric congeners may offer
insight into some of the basic traits of weedy exotics
(Schierenbeck et a1. 1994).

Pueraria lobata, C. orbiculatus and L. japonica are
native to Japan, Korea and eastern China. celastrus
orbiculatus and L. japonica thrive even where freezing
conditions are common. All three were introduced to Nerth
America on purpose, yet the outcomes were unanticipated
though even Darwin (1859) was aware of the potential response
of species released from their native constraints. The
introduction of C. orbiculatus can be taken as an example.
celastrus orbiculatus was introduced to the US from Asia in
1860 as a control measure against erosion and as an
ornamental plant. During the period of 1966 and 1967 the
National Arboretum.sent seeds of C. orbiculatus to nurseries
in 30 states. By 1970, C. orbiculatus was planted as an
ornamental in 33 states and.was reported to be naturalized in
21 states. (Patterson 1974). By the 19805, C. orbiculatus was
considered a problem weed (Dreyer et a1. 1987, Robinson et

al. 1994, Goslee 1998).

The weedy nature of C. orbiculatus may be related to its
reproductive success. Dreyer et al. (1987) compared pollen
viability and seed germination in C. orbiculatus and C.
scandens. The native C. scandens has decreased in abundance
in part due to overcollecting by hobbyists (Rabeler 1998). At
the same time, C. orbiculatus has been increasing in
distribution. It would be valuable to know if this decrease
has in part been influenced by or is merely concomitant with
the invasion of the exotic species. Dreyer et al. (1987)
found that the pollen of C. orbiculatus had higher viability
than C. scandens (67% and 48%, respectively). Additionally,
the seed germination rate of C. orbiculatus was greater than
C. scandens (71% and 27%, respectively). Much of the success
of C. orbiculatus over C. scandens can be understood using
reproductive explanations.

A species newly established in a community may be too
foreign to the local fauna to be recognized as a resource.
This may lead to lower herbivory compared to that experienced
by the native species, thereby giving the exotic species an
advantage. Schierenbeck et al. (1994) found this to be the
case with the exotic liana L. japonica and its native
sympatric congener L. sempervirens. Lonicera sempervirens
suffered greater damage due to herbivory and had lower total
biomass accumulation than L. japonica. Lonicera japonica not

only suffered less herbivory but it demonstrated a

compensatory response to the low levels it experienced. This
favors the growth and spread of L. japonica where the two
species grow in sympatry (Schierenbeck et al., 1994).

Vines use a variety of different mechanisms to climb,
including twining up stems and specialized tendrils. The
mechanism utilized in part dictates the size of the substrate
that the liana can successfully climb, and therefore also
determines the light available to the growing vine. Carter
and Teramura (1988) compared climbing mechanism and.vine
photosynthesis. They found that the exotic twiner P. lobata
was best suited to full light, but performed poorly in low
light. The exotic twiner Lonicera japonica, native tendril
climbers (Parthenocissus quinquefblia, Vitis vulpina, smilax
rotundifolia) and adhesive root climbers (Hedera helix, Rhus
radicans) were better suited to the low light levels of the
understory. However, under full sunlight Parthenocissus
quinquefblia, Vitis vulpina, and smilax rotundifolia
increased photosynthetic capacities. Since L. japonica is
evergreen in the southeastern US and can utilize sun flecks,
it may be problematic in low light environments. Celastrus
orbiculatus also has been shown to have a wide tolerance of
light levels and increased response to high light (Patterson
1974). These findings indicate that exotic lianas utilize

different light—use strategies; that there is not one single

10

key to success, and that there is a range of physiological
plasticity in some liana species. (Carter & Teramura 1988).

Carter et al. (1989) further established that simple
high photosynthetic capacity is not responsible for the
success of exotic lianas. They demonstrated that under field
conditions, the steady-state photosynthesis was similar
between exotic Pueraria lobata and Lonicera japonica and
native Parthenocissus quinquefOlia, Vitis vulpina and
Clematis virginiana. Additionally, under high leaf-air water
vapor pressure differences common at high temperatures,
photosynthetic rates decreased more in the exotic lianas than
several of the natives (Carter et al. 1989). Their results
indicate that steady-state photosynthesis is not the simple
answer explaining the weedy nature of these exotic lianas.
However, mechanisms such as maintaining optimal leaf
temperature through conductance and transpiration may give
exotics like P. lobata an advantage over native

species(Forseth & Teramura 1987).

Case Studies: Community invasions by exotic lianas

Robertson et al. (1994) examined the colonization
dynamics of exotic species on a northern piedmont in
Pennsylvania. Included in their study were two true climbing
lianas (L. japonica and C. orbiculatus) and one scrambling

vine (Rosa multiflora). Density and frequency data were

11

collected for each species in different successional
communities. Lonicera japonica was by far the most frequent
invader, present in 75% of all plots. Rosa multiflora was the
second most frequent, though it was less successful in mature
forest and old field plots. celastrus orbiculatus presence
did not differ between seral stages (Robertson et al. 1994).
The mature forest had the lowest frequency and density of
exotic species. Only C. orbiculatus and L. japonica were
found in the mature forest to any degree (39% and 48% of
plots, respectively). This is probably due to the ability of
C. orbiculatus to germinate under low light conditions
(Patterson 1974, Dryer et al. 1987) and L. japonica to remain
somewhat evergreen (Carter & Teramura 1988). Additionally,
this study may be evidence that mature forest tends to be
relatively exotic free because it suffers less physical
disturbance (Robertson et al. 1994).

When a community is subjected to high levels of
disturbance, the native flora can be significantly altered,
making room for invasion. RObinson et al. (1994) looked at
the change in flora of Staten Island over 112 years. During
this time 443 native species were lost and more than 100
alien species were naturalized. The only traits correlated to
the loss of native species were that herbaceous and uncommon

species were more likely to be lost. Among the naturalized

12

aliens were the exotic lianas C. orbiculatus, P. lobata and
L. japonica.

The New Zealand flora is already largely comprised of
alien species. Each wave of human settlers brought with them
their favorite plant species, including agronomic and
ornamental plants. The introduced species often escaped and
became naturalized. By the tens rule, approximately 146,300
species introductions have occurred in New Zealand in the
last 133 years! Baars and Kelly (1996) compared growth
responses to light availability in introduced and native
vines. Two of the introduced vines (Clematis vitalba and
Lonicera japonica) displayed low light compensation points as
well as high relative growth rates in the presence of high
light availability. The third introduced vine (Passiflora
mollissima) was more similar to a native vine (Muehlenbeckia
australis): higher light compensation point and higher
requirement of light availability for maximum growth rate. A
final native vine (Parsonsia heterophyila) had the lowest
light compensation point and also the lowest maximum.growth
rate. This study demonstrates the wide variety of strategies
for exotic lianas in varying light environments. It may be

that for every community, there is a corresponding invader.

13

Conclusion

Any community is theoretically invadable, since all
communities have at least some probability of disturbance.
Whether an invasion occurs depends on the timing of
disturbance and dispersal of the invader. Human activities
have increased the frequency of disturbance as well as the
relative rates of species introductions through global
travel, so high invasion rates would not be surprising.

Exotic lianas pose a real threat to temperate
communities because there are fewer native lianas with which
to compete. The native Michigan flora may be at particular
risk from exotic lianas, since only 1% of the native flora
are lianas. This suggests that the climbing strategy is
currently underutilized in Michigan. Historically, the
depauperate Michigan liana flora may relate to habitat
resistance to lianas and therefore little opportunity to
diversify. Currently, however, exotic lianas have the
potential to proliferate through disturbed habitats with open
liana niches. The ruderal traits outlined by Grime (1979) are
a good start for characterizing these weedy pests. However,
further studies comparing exotic weedy and native non-weedy
congeners will help define more traits common among pests.

These traits will be essential for modeling forest community

14

CHAPTERZ
Cblastrus orbiculatus (Oriental bittersweet) natural history

and presence in Michigan

Introduction

The spread of exotic, invasive plant species continues
to threaten native floras (Groves & Burdon 1986, Mooney and
Drake 1986, Drake et al. 1989, Cronk and Fuller 1995, Pysek
et a1. 1995). Celastrus orbiculatus is one such species
becoming a problem weed in Michigan (Voss 1985, Tibbetts and
Ewers 2000). This liana (woody vine) may be locally more
abundant than the native congener C. scandens. Reliable
identification can be made based upon inflorescence position:
terminal panicles in C. scandens, axillary cymes in C.
orbiculatus (Voss 1985). An understanding of the natural
history and invasion history of C. orbiculatus may help us

combat such threats.

Taxonomy
Celastrus orbiculatus Thunb. (Oriental bittersweet) is a
woody twining vine native to north and central Japan, Korea,
and China (Hou 1955). It is a member of the Celastraceae, the
Bittersweet or Staff Tree Family. The most recent revision of
the genus Celastrus is by Hou (1955). The generic name traces

back to Theophrastos, who assigned the name Kelastros to an

15

evergreen tree (Phyllyrea = Phillyrea, Hooker and Jackson
1895). This tree is not a member of the Celastraceae, but
instead is found in the Oleaceae, its members distributed
around the Mediterranean (Mabberly 1997). In his designation
of the name Kelastros, Theophrastos used the feminine
gender. Linnaeus founded the genus celastrus as it is now
understood in his Genera Plantarum (1960), changing the
gender from feminine as it applied to Phyllyrea to masculine .
for his circumscription. The International Code of Botanical
Nomenclature (ICBN) requires that such borrowed Greek or
Roman names revert to their classical gender for authors
following Linnaeus. However, some authors (e.g., Voss 1985)
have used the feminine celastrus orbiculata over C.
orbiculatus following its assignation by Theophrastos. This
helps explain some of the synonymy and confusion over species
names within the genus.

There is additional confusion regarding the correct name
of the species Celastrus orbiculatus. Thunberg (1784)
described this species in his Flora of Japan. Apparently
Thunberg assigned the name C. orbiculatus in his manuscript
and figures, but a printer’s error substituted C. articulatus
in its place (Maximowicz 1881). However, C. articulatus was
already widely accepted, and not easily replaced with the
correct C. orbiculatus. Now, C. orbiculatus has generally

replaced C. articulatus, probably aided by the fact that the

16

epithet orbiculatus descriptively refers to the leaf shape.
However, there is still evidence of nomenclatural inertia as
demonstrated by some recent publications (e.g., Osipova 1982,

Shokova and Belinskaya 1987).

Distribution of the Genus

The 31 recognized species of Celastrus are currently
found in eastern Asia, Oceania, North and South America, and
Madagascar (Hou 1955). They are predominately tropical and
subtropical. Berry (1919) indicates that the fossil evidence
points to a widespread, abundant cosmopolitan distribution
during the Tertiary. Considering the present distribution
patterns, Hou (1955) suggests two centers of dispersal:
Yunnan-Burma-eastern India (Asiatic center), and Central
America, corresponding to subgenus celastrus and subgenus
Racemocelastrus, respectively. The one North American native
member of the genus, celastrus scandens L. (American
bittersweet), apparently has closer affinity to the eastern
Asiatic center of dispersal, and falls in subgenus Celastrus.
The subgenera differ in diversity, with subgenus celastrus
including 24 species and subgenus Racemocelastrus only 7
species. Species of subgenus celastrus have two ovules per
ovary cell and is dioecious, while subgenus Racemocelastrus

has one ovule per ovary cell and is bisexual (Hou 1955).

17

The distribution of the species of celastrus appears to
be an example of the disjunct distribution between eastern
Asia and eastern North America seen in numerous taxa: e.g.
Rhododendron (Kron 1993), Panax (Wen and Zimmer 1996),
Trillium (Fukuda 1990), Acer (Hasebe, Ando and Iwatsuki
1998). Li (1952) describes the disjunction as the loss of a
continuous mesophytic forest spanning the northern hemisphere
during the Tertiary, and subsequent diversification within
each region. However, the biogeographic pattern of some taxa
(e.g., Liquidambar and Staphylea) may be due to exchange

along contiguous land bridges (Wen 1998).

Biology

Morphologically, C. orbiculatus and C. scandens, both of
subgenus Celastrus, are very similar. The leaf form.and
margin crenulation intergrade between the species. The main
difference used to distinguish the two is the inflorescence:
axillary cymes for C. orbiculatus and terminal panicles for
C. scandens. Both species are dioecious to polygamodioecious.
The gynoecium is usually 3 carpellate (sometimes 4), 3-
locular, with 2 (1) ovules per locule. The fruit is a small
(1 cm) orange to yellow subglobular leathery capsule. It is
incompletely 3-locular, 3 valved, with 2 (1) seeds per
locule. Seeds of both species have c0pious endosperm, and 2n

= 46 for each (Brizicky 1964, Gleason and Cronquist 1991).

18

Viable hybrids between the two species have been produced;
these resemble C. orbiculatus in morphology but are of lower
vigor (White and Bowden 1947). The seeds are enclosed in a
fleshy red aril that is exposed upon reflexing of the valves
in autumn, and birds disperse the seeds of both species. Both
species are also capable of vegetative propagation from root

sprouts.

Ecology in native range

There is little ecological information regarding C.
orbiculatus in its native range. Ohwi (1965) characterizes
the habitat as “thickets and grassy slopes in lowlands and
mountains," and the abundance as “common and often planted as
a hedge." Patterson (1974) reports that C. orbiculatus is not
a weed in Japan. A report of vine infestation of a
Chamaecyparis obtusa plantation in Japan found C. orbiculatus
climbing the planted trees in only one of seven stands,
though it was present on the forest floor in five other
stands (Suzuki 1984). This may be considered analogous to the
situation with C. scandens which has been found to create
only occasional problems in North American silviculture (Lutz
1943).

Celastrus orbiculatus is a plant used in traditional
Chinese medicine. Screening for central nervous system

activity of plant extracts has shown that C. orbiculatus has

19

some strong binding to receptors in radioligand receptor
binding assays, perhaps indicating the functional action for
its traditional use (Zhu et al. 1996, Phillipson 1999).
Additionally, in the search for substitutes to calf rennet
for cheese making, milk-clotting activity has been found in
leaf extracts of C. orbiculatus (Otani, Iwagaki and Hosono
1991).

Both C. orbiculatus and C. scandens have been used in
decorative arts. Each species produces bright yellow-orange
capsules that open to reveal red-aril covered seeds. In
Japan, C. orbiculatus is collected and sold in autumn
(Sargent 1893). Michigan Public Act 182 of 1962, also known
as the “Christmas-tree law," includes C. scandens in the list
of species protected from.over-collection by avid decorators
(Rabeler 1998).

There is sparse information regarding either pests or
diseases affecting C. orbiculatus, either in its native range
or in North America. There is evidence that insect herbivores
utilize C. orbiculatus. Cotton aphids, Aphis gossypii Glover,
feeding on C. orbiculatus in Japan were found to have lower
resistance to organophosphorus insecticide (Saito 1989). In
Michigan, Kiss (1984) reported a phloemrfeeding membracid
nymph of the Ehchenopa binotata (Say) complex that feeds on
several host species including C. orbiculatus, C. scandens,

JUglans nigra, J; cinerea, and several species of Viburnum.

20

No mention of mortality related to feeding on celastrus is
mentioned (Kiss 1984). Tomato black ring virus (TBRV) was
reported to spontaneously occur on C. orbiculatus (Schmelzer
1974).

Introduction to Nbrth America

Celastrus orbiculatus was introduced to North America
as an ornamental vine around 1860 (Patterson 1974). The exact
date of introduction remains confused by several different
accounts and records. Seedlings of C. orbiculatus were being
cultivated at the Arnold Arboretum and the New York Botanical
Garden and had become quite popular in landscaping by the
1890s (Sargent 1890, Nash 1919, wyman 1949; for a synopsis
see Patterson 1974).

From the initial plantings, it was observed that the
plant grew rapidly, aggressively, was hardy, and was
therefore desirable as a cover plant (Jack 1989, Sargent
1890). The greatest concentration of early C. orbiculatus
appears to be in the northeastern United States (Patterson
1974). Naturalized.populations are noted from.1912 (Maryland)
and 1916 (Pennsylvania and Connecticut) (Mehrhoff 1986,
Patterson 1974). A survey of herbaria by Patterson (1974)
demonstrated that C. orbiculatus had become naturalized in at
least 21 of 33 states where it had been planted. Celastrus
orbiculatus was planted along highways in New Jersey, Rhode

Island and Massachusetts, and seeds were distributed to 30

21

states by the National Arboretum in 1966-1967 (Patterson
1974).

Celastrus orbiculatus has also spread to other parts of
the world. Collections have been reported in Berlin and
Seeheim, Germany (Bolle 1894, HillesheimrKimmel 1995). In
Russia, C. orbiculatus has been noted as well—suited to the
hot and arid climate of Kazakhstan, and is not negatively
impacted by the high sulphur dioxide pollution levels

(Shokova and Belinskaya 1987).

Status in Michigan

The earliest floras of Michigan, particularly the
southern Lower Peninsula, indicate that C. orbiculatus was
not present, but its native congener C. scandens was (Beal
and Wheeler 1892, Beal 1904, Gleason 1939, Walpole 1924,
Hanes and Hanes 1947). Celastrus scandens is considered
native to North America (Hou 1955), and is reported as
occurring frequently in these early floras. Throughout
Michigan this species is present in 52 counties including
both the Upper and Lower Peninsulas (Voss 1985). However, it
has decreased in abundance in part due to overcollecting by
hobbyists (Rabeler 1998).

At the time of Patterson’s (1974) survey, C. orbiculatus
was being cultivated in Michigan but had not been reported to

have escaped. Voss (1985) noted C. orbiculatus as present in

22

three counties of southern Michigan (Figure 2-1, Berrien, St.
Joseph, Washtenaw). However, it has been collected further
north since Voss’ publication (Figure 2—2, Lenawee,
Kalamazoo, Barry, Ingham, pers. obs.; Kent, Wayne, Voss,
pers. coma) and is probably grossly undercollected (Voss,
pers. com"). The increase in distribution over 15 years is
notable, particularly the expansion to the north. This
species is reported as hardy in Zone 4 (Wyman 1949). While
Patterson (1974) reported that C. orbiculatus had spread to
most of the states in its potential range east of the
Mississippi, it is clearly still spreading within these
states. Careful identification, monitoring, and swift removal
are recommended in dealing with this species (McNab 1988).
For landscaping purposes, use of the native C. scandens is

highly preferred.

Species used in the research

Direct comparison of the ecology of the exotic C.
orbiculatus and the native C. scandens would be the ideal
approach to elucidating explanations for the invasive nature
of C. orbiculatus. The habitat ranges for both species
overlap, so theoretically they should be found naturally co-
occurring. However, in numerous field examinations of
reported C. scandens collection sites, this species was not

found. In some instances, C. orbiculatus was present instead

23

of the reported C. scandens, suggesting misidentification of
the herbarium.specimen. Replacement of C. scandens by C.
orbiculatus is another possibility. In many other instances,
neither species was present, sugesting local extinction of
the native C. scandens. Celastrus scandens and C. orbiculatus
were never found naturally co-occurring in the field.
Investigation by Patterson (1974) into the potential of
allelopathy by C. orbiculatus failed to detect any such
interaction. Overall, C. scandens sites were infrequent at
best and limited in extent.

To overcome the lack of C. scandens sites, and to avoid
further threatening this protected species, another native
liana species was used as a substitute for several of the
following investigations. Vitis riparia Michaux (riverbank
grape) was utilized in studies requiring destructive sampling
and pairwise comparisons with C. orbiculatus, since both
species could be found co-occurring. This substitution was
felt to be relevant because V; riparia and C. scandens are
commonly found in similar habitats and share a similar
distribution throughout Michigan (Figures 2-3, 2-4)(Voss

1985).

24

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Figure 2-1. Celastrus orbiculatus distribution, 1985 (after
Voss 1985).

25

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Figure 2—2. Celastrus orbiculatus distribution, 2000.

26

 

 

 

 

 

 

 

Figure 2—3. Celastrus scandens distribution (after Voss
1985) .

27

 

 

Figure 2-4. Vitis riparia distribution, (after Voss 1985) .

28

CHAPTER 3
Root pressure and specific conductivity in temperate lianas:
exotic Cblastrus orbiculatus (Celastraceae) vs. native Vitis

riparia (Vitaceae)

Introduction

Lianas (woody vines) comprise ~1% of the Michigan flora
(29 species of a total of 2465 as reported by Voss 1972,
1985, 1996). Native lianas, e.g., Parthenocissus, Vitis, and
Tbxicodendron, are capable of reaching the tops of tall trees
and shading out their hosts. These vines rarely develop into
thick monospecific stands that exclude other non-tree
species. However, some exotic vines have become weeds,
capable of extensive infestations that may affect community
structure (Penfound 1966). Pueraria lobata (kudzu) is one
such vine common in the southeastern united States (Wechsler
1977), while another, celastrus orbiculatus (Oriental
bittersweet), appears as far north as Michigan and
Connecticut (Patterson 1974). celastrus orbiculatus is native
to China, Japan and Korea (Hou 1955). Exotic species may
proliferate for various reasons such as escape from their
native herbivores, pathogens, and seed predators, as well as
enhanced growth in novel environments. I was interested in

examining whether water transport properties could.be

29

implicated in the success of celastrus orbiculatus over Vitis
riparia in Michigan.

Lianas are much more prevalent in tropical than in
temperate ecosystems, both in terms of biomass and as a
percentage of species in the flora (Gentry 1991). It has been
suggested (Ewers 1985, Sperry and Sullivan 1992) that low
temperature limits the distribution of lianas, possibly via
freeze-induced air bubble formation in xylem vessels. When
the water in the vessels freezes, the solubility of dissolved
gases decreases and bubbles form" If thawing occurs more
rapidly than the air can redissolve, the bubbles remain and
may increase in size due to the tension of the transpiration
stream.(zimmermann 1983). These air bubbles (emboli) occlude
the vessels and prevent further conductance of water. The.
likelihood of embolism occurring due to freezing increases
with vessel diameter (Sperry and Sullivan 1992, Davis and
Sperry 1999), and vines characteristically have wide vessels.

Embolism.may also be caused by water stress. Air may
enter conductive vessels through intervessel pit membranes as
the xylem pressure decreases (Sperry and Tyree 1988). This
relationship can be expressed as a vulnerability curve,
showing an increase in embolism as xylem pressure decreases.
This vulnerability curve has been shown to be characteristic
for given species and can be informative regarding likely

species response to the xylem pressures typically experienced

30

by the species under field conditions (Sperry, Tyree, and
Donnelly 1988; Davis et al. 1999).

Root pressure may be a repair mechanism of plants with
wide vessels, such as lianas, that are at high risk of winter
embolism” Without a mechanism to remove emboli, vessels will
remain permanently dysfunctional. Root pressure is one manner
by which conductance can be restored in embolized vessels.
Water is taken into the roots osmotically and then forced up
through the plant. Emboli may be quickly pushed out by the
water, pushed through dry pit membranes, or more slowly
dissolved when pit membranes are wetted (Sperry et a1. 1987).
Examples of positive root pressure include the exudation of
water through hydathodes (guttation) and the “bleeding" of
severed stems. These occurrences are generally limited to
conditions of minimal transpiration, such as before dawn,
when the stomata are closed, and during periods when relative
humidity is at or near 100%, such as during rain. Positive
root pressure has been observed in many plants, such as Vitis
(Sperry et al. 1987), Acer (Sperry, Donnelly, and Tyree
1988b), and many tropical species (Ewers, Cochard, and Tyree
1997; Fisher et al. 1997).

The risk of dysfunction may be balanced by a high
hydraulic conductivity in stems with xylem dominated by wide

vessels (Chiu and Ewers 1992; Ewers, Cochard, and Tyree

1997). Hydraulic conductivity (kh) is measured as the volume

31

of water transported through a unit length of stem.per unit

time divided by the pressure gradient. Specific conductivity

(ks) is kh per unit cross-sectional area of the xylem and

reflects the efficiency of water transport (Tyree and Ewers
1996). Liana stems provide little mechanical support, are
generally narrow with respect to the leaf area they supply
(Ewers 1985, Ewers and Fisher 1991), contain wide vessels,

and are primarily committed to water transport; therefore

they typically have high ks values.

The wide vessels of lianas should be prone to
dysfunction when temperatures fall below 0°C, yet some lianas
thrive in temperate climates and.persist despite freezing.
The best studied temperate lianas in this regard are Vitis
riparia and Vitis labrusca L., and several authors have
suggested that the success of wide-vesseled temperate lianas
may depend upon root pressures (Sperry et al. 1987; Sperry,
Donnelly, and Tyree 1988b; Ewers, Cochard, and Tyree 1997;
Fisher et al. 1997). The objective of this study was to
investigate whether differences in water transport
characteristics were sufficient to explain the differences in
growth patterns of C. orbiculatus vs. V: riparia. I
hypothesized that in co—occurring species, plants of C.

orbiculatus would have: (1) stronger or more persistent root

pressures, (2) higher ks values through much of the season,

32

and (3) would be less vulnerable to embolism caused by water

stress than the co—occurring native species V1 riparia.

Methods and Materials

§i§§-- Field sites were chosen based on their proximity
to laboratory facilities and the presence of both V1 riparia
Michaux and C. orbiculatus Thunb. at each site. Plant
specimens were selected based on healthy appearance and stem
diameters between 1 and 3 cm” Four sites were used, which
were all within a 130-km radius of the Michigan State
university (MSU) campus, where all laboratory measurements
were made. Site locations are described in Table 3-1.

Root pressure-- Root pressure was measured on individual
specimens at two sites with bubble manometers (Sperry 1983;
Ewers, Cochard, and Tyree 1997; Fisher et al. 1997). Five
healthy individuals for each species were selected, with stem
diameters between 1 and 3 cmr The day prior to measurement,
stems were cut and manometers containing distilled water and
a distal air bubble were attached. The next day, air bubble
length pre- and post— attachment to the severed stems was
recorded just before sunrise to avoid the effects of
transpiration. Root pressure in kiloPascals was calculated

using the formula (Fisher et al. 1997):

33

modaamm othB oflmmfi .pmxflfi .%©CMm Hm>o hEmoHumnflm Hmm Mmm mmB
DmmHow mammzusowmm soumfla
Awqmv mcmpnmw mxmq Cmppflm

«\Hmm «\sz mam 3am Zea
mmamsvmsnoo oeumd oemmfi .Umxfle .hfimoauwcflm onwmcmq Dmmm
moaomom was nonfiosm sues .pamfim HMGOflmmmUUSm penvaszv hoflmum>HCD minim someone:

¢\H3m ¢\H3m mmm Mam ZdB

mmaopoamom oeuonommoaw canoe .UMXeE .hsooHanem cosmeoeaaez
msnm nuw3 .Uamem HosoemeUUSm UHO Show Hmcnmm

N\H3 v\HZZ mmm mam Zwfi

 

mmampoamom ofimhe venue .owxdfi .hfimoHummumoo soogfioeaafiz
coasticmHQ meuumm>ahw wooed uoeamuma Show mopeuumm
Heom\soeuaenommp coaumuoa\muflm

.somflsoez Ge mmuew monum on» mo some Ge usmmmum maeom one mummy
ummMOM on» mo mCOfluQeuommp one .wsoeuMUOH .mwfioz .mCOfiumeuomwp muflm .Hnm magma

34

px = 100[(Latm/Lpd) - 1]

where E; = xylem.water pressure, La

tm = bubble length in

manometer at atmospheric pressure, anded = bubble length

prior to dawn.

Specific conductivity—- Specific conductivity of both
species was measured in 1996 and 1997, on stems collected
from each of the four sites on a revolving schedule. Each
site was sampled at least once a month in the spring and
summer, and less frequently in the winter. On each collection
date, stems of five individuals for each species were severed
under distilled water in the field. Measurements were made in
the laboratory following the method of Sperry et al. (1988a)

and modified according to Chiu and Ewers (1992). Field

condition kh was measured on 10-cmrlong segments with a

pressure head always less than 1.5 kPa. Stem.segments were

then flushed at 172 kPa for 20 min, and final kh (=maximum)

was determined when repeated flushing yielded no increase in
conductivity.

Following the conductivity measurements, all stems were
perfused with a 0.5% crystal violet dye solution to mark the
conductive vessels. A 5-cm column of dye of the same diameter
as the stem was allowed to perfuse through the flushed

segments. The time required for dye to reach the distal end

35

of the stem.segments was noted. Stem.segments adjacent to
those used for conductivity measurements served as field
condition controls for dye descents. All the field condition
control stems were then perfused with the dye eight times
longer to insure that even some of the smaller vessels could
potentially pass the dye. After perfusion with dye, the stems
were perfused with distilled water a minimum of 15 min to
prevent bleeding of dye from conductive to nonconductive
vessels.

After perfusion and drying, each stem.segment was
severed 2 cm from the proximal end (perfusion port) and
shaved smooth with a razor blade. The dyed growth rings and
total growth rings were counted using a dissecting
microscope. A growth ring was considered conductive if it had
five or more stained vessels.

Sapwood area, as demarcated by the dyes in transverse
view, was measured using a caliper with a digital micrometer.
Bark was removed, and the maximum and minimum xylem diameters
were averaged and used to calculate the xylem cross—sectional
area. The pith and heartwood area, demarcated by a lack of
dye, was also measured and subtracted from.the xylem area to

obtain the area of conductive xylem. The field condition and

maximum.kh values calculated above were divided by the

conductive xylem area to obtain kS values. The percentage

36

embolism was taken as the difference between maximum.ks and

initial ks! and standardized by dividing by the maximum.ks.

The conductivity data obtained were plotted against date
and phenological data collected throughout the year to
determine whether the relationship varied between the two
species. Phenological data were summarized for all sites and
included date of bud break, leaf out (first leaf fully
expanded), flowering, and first leaf drop.

Vessel diameter measurements—- Two stems for each
species were used to determine the distribution of vessel
diameters. The tangential diameters of all vessels in four
equivalent quadrants per stem were measured in transverse
view with an Optical micrometer. Quadrants were bounded by
rays. vessel diameter distributions were compared with an
unpaired, two-tailed t test. Theoretical conductivity was
calculated for each vessel diameter class using the Hagen-
Poiseuille equation following Chiu and Ewers (1992).

The maximum.tangential diameter in transverse view was
recorded for the ten largest vessels in these distributions.
Maximum.vessel diameter between the two species was compared
with an unpaired, two-tailed t test.

vulnerability curye§—- Stems were cut in the field
between July and October 1997, transported to the laboratory,

and allowed to dehydrate for various lengths of time (N'= 30

37

for C. orbiculatus,.N = 5 for V3 riparia). The stems were
then bagged and allowed to equilibrate in the bags overnight
following Sperry, Donnelly, and Tyree (1988a). Stem segments
were cut to be longer than the maximum vessel lengths. The
mean xylem pressure was determined using a pressure bomb on
five shoots from each stem.after equilibration. The stem
segments were then severed under water into ten 10—cm
lengths. Specific conductivity and percentage embolism were

detenmined as described above.

Results

In undertaking this study I expected to find differences
between the two species that would relate to the success of
C. orbiculatus as an invasive weed. I found that only V1
riparia frequently demonstrated.measurable root pressure
during both 1996 and 1997 (Figure 3-1). Root pressure was
greatest early in the spring, then declined into summer.

Celastrus orbiculatus had almost no measurable root
pressures (Figure 3—1). Positive, but minor root pressures
were observed on a very few occasions. Large air bubbles were
frequently observed in the manometers, indicating negative
pressure. However, the bubble manometer method is not
reliable for negative pressures, so these values were

considered no different from zero (Ewers et al. 1997).

38

 

125
1001 V
75-

50‘

 

N
Ul
l
+—|o=t0-—i
o—a
.1
l—-O—-i

2

 

 

 

 

 

 

 

 

 

 

 

 

 

73
Q4
'5 O r c
a) -25 r I I I
H APR MAY JUN JUL AUG
:3
(a 125
8 100:3 _r .. 0 V. riparia
Ll
9' _ 0 C. orbiculatus
*J 75 O C)
8
H 50 y i
25" O T
l o
o H c Gee—9+ 9
_25 i I I l
JAPR. NHUI CHinS JR”; ARK}
x u a
date 8 3 5
H )4
Q ‘44 (l)
to 3
'3 .3 .9.
Q ‘H

Figure 3-1. Root pressure. (A) 1996. (B) 1997. Each
symbol represents the mean for five stems. The range
for V1 riparia is 0—145kPa. Error bars represent +/- 1
SE. Where error bars are not visible, they are smaller
than the plotted symbol. Relative phenological events
are indicated by arrows (white arrows = V; riparia and
black arrows = C. orbiculatus).

39

 

Despite differences in site characteristics, the trends
in conductivity were relatively uniform across sites for both
species. In 1996, V; riparia reached its minimum percentage
embolism sooner than C. orbiculatus (Figure 3—2A). The
minimum percentage embolism in V3 riparia (37%) was reached
by the beginning of June, whereas in C. orbiculatus the
minimum (50%) occurred at the end of August. The reduction in
embolism began prior to leaf out in V1 riparia, but it did
not occur until after leaf out and after maturation of new
vessels in C. orbiculatus.

Both species produced flowers and fruit at roughly the
same time. Leaf fall in V1 riparia roughly coincided with
increased embolism and the first daily minimum temperatures
belOW'OOC. The leaves of C. orbiculatus remained green at some
sites for over a month beyond the first frost. During the
winter of 1996-1997, embolism reached 100% in both species.

The same general patterns were observed in 1997. Vitis
riparia reached its minimum percentage embolism sooner than
C. orbiculatus (Figure 3-2B), however, for both species the
period of reduced embolism began about one month earlier than
in 1996, and therefore the total period of reduced embolism
lasted longer than in 1996. In both species minimum embolism
was slightly lower in 1997 than in 1996, and did not occur
until one month later. The minimum percentage embolism

reached during 1997 for V; riparia was 29% during August,

40

 

 

 

 

 

 

 

 

 

 

 

U
A a 3 :3 :3 t:
a 100‘ ' ' '
m o e 9‘ 3' ?:5
H 75.. I: O L0
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257 “2|. 0 V. riparia
0 C. orbiculatus
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(1) ragg- ' o 31
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op C’o T .I.
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(5 JJ 5’ Q:
a, :3 .G 0
date 35 ° {1 «a
(H (D
"C to 5 it;
3 3 a 2
Figure 3-2. Percentage embolism” (A) 1996. (B) 1997.

Each symbol represents the mean for five stems. Error
bars represent +/- 1 SE. Where error bars are not

visible,

they are smaller than the plotted symbol.

Relative phenological events are indicated by arrows

(white arrows

V; riparia and black arrows

C.

orbiculatus). Some relevant mdnimum.daily temperatures

are indicated along the top.

41

while for C. orbiculatus it was 42% during October. Unlike
the winter of 1996-1997, embolism failed to reach 100% during
the winter of 1997—1998 and, therefore, reduced embolism
persisted for a longer time.

Vitis riparia achieved rates of initial (=native)
specific conductivity about two to four times higher than C.
orbiculatus (Figure 3—3). The peak values (i 1 SE) for V.
riparia in 1996 were 49.4 i 10.3, and for 1997 64.8 i 20.1 kg

2

° 5‘1 0 MPa * m.m’. For C. orbiculatus, the values were 17.9 i

5.7 in 1996, and for 1997 21.0 i 3.5 kg 0 s“1 0 MPa 4 m m”.

Similarly, the final ks, measured after flushing the stems,

was consistently higher in V1 riparia than in C. orbiculatus
(Figure 3—4). These values did not show a clear seasonal
trend in 1996, although in 1997 the values peaked in July for
C. orbiculatus.

Stems sampled for conductivity measurements ranged
between 5 and 12 mm in diameter. During 1997, the mean stem
diameter (i 1 SE) for V1 riparia was 7.5 i 0.1 mm (N'= 145)
and for C. orbiculatus 8.1 i 0.1 mm (N'= 145). The difference
in stem diameter was significant (two-tailed t test, P =
0.0002). However, the mean stem age (i 1 SE) for V3 riparia
was 4.2 i 0.2 yr. (N'= 140) and for C. orbiculatus 3.7 i 0.1
yr. (N = 140). The difference in stem age was significant

(two-tailed t test, P = 0.03).

42

 

 

 

 

 

 

 

 

 

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F Id AI :M J' J IX

 

 

 

 

 

S C) IN

I I
ID

100
A V. riparia
75- C. orbiculatus
A T
(Tam Ifi°
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l- O T -T o
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g i I 3' I a 'fi 8 £091:
:3 0‘ " I I I ‘
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.54 ..
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.52. i Tmfiil T
T010 0.;
Eon-[7L0 J- § ..
.K>:; -..q. I. a: g
0 PM... "I—r93 '- 4'

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Figure 3-3. Initial (native) specific conductivity (ks).

(A) 1996.

(B) 1997. Each symbol represents the mean for

five stems. Error bars represent +/- 1 SE. Where error
bars are not visible,

symbol.

they are smaller than the plotted

125

 

 

 

 

 

 

 

 

 

 

A 0 V. riparia
loo-J T O C. orbiculatus
° 6 T T'I' T
o
754 ‘I'T I 11 $06 1)
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,4 Ti 3 1' JI‘J. T i o T
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25_ . 1.35 IOIDT. l, 3' l. O
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. .2 $1" .‘
O I I I I I I I I I I fl I I
J’ F II A. II J' (J .A 53 0 DJ D J'

date

Figure 3-4. Final (maximum) specific conductivity (ks).

(A) 1996. (B) 1997. Each symbol represents the mean for
five stems. Error bars represent +/- 1 SE. Where error
bars are not visible, they are smaller than the plotted

symbol .

44

The number of active growth rings differed between the two
species (Figure 3-5). Stems of V; riparia routinely showed
that in their native state (without removal of emboli),
several growth rings contributed to the stem conductivity
(Figures 3—7 and 3—11), with about two to four conductive
growth rings by the end of April (Figure 3-7). However, for
C. orbiculatus rarely more than one growth ring was capable
of conductance (Figures 3—6 and 3-10). High pressure flushing
to remove emboli induced conductance in additional growth
rings in C. orbiculatus (Figures 3-8 and 3-12), but not in V.
riparia (Figures 3-9 and 3—13).

The distributions of vessel diameters of the two species
are remarkably similar (P > 0.9, Figure 3—14). Both species
have a large number of narrow diameter vessels that
contribute little to the theoretical conductivity. However,
the four largest vessel diameter categories (<160 um) are
responsible for ~63% of the theoretical conductivity, though
numerically they only represent 8% of the total vessels in
the stems of each species. The average maximum.vessel
tangential diameter (i 1 SE) for C. orbiculatus was 203 i 6
um, and for V1 riparia 191 i 3 um. This difference was not
statistically significant (P = 0.08), despite the wood of C.
orbiculatus being ring-porous and that of V1 riparia diffuse-

porous.

45

 

 

 

 

 

 

U) 6

.5: 1997 0 V. riparia

H 5" I ' C. orbiculatus
:3 F .

I4- I

m T° I; a

23* 1 ° 1 1,13“ T *

.,_| O

8 2- 1 111; T1: OI: IE I

f, 1111;). 1.1 o l
01. T “.m. .Li 1
H I 1 T

a) 1r 1

g. i eat-1 5
Q FIM A MIJTJIAISIOfiNrD—IJT

date

Figure 3-5. Number of active growth rings. Error bars
represent +/— 1 SE. Where error bars are not visible,
they are smaller than the plotted symbol.

46

Figures 3—6 to 3-13. Transverse view of stems. Scale bar
= 200 um and applies to all figures. Perfusion of stems with
crystal-violet—marked conductive vessels. Stems were
collected from the same site on two different dates. Figures
3—6 to 3-9, stems collected on 30 April 1997. 3-6. Celastrus
orbiculatus, native state. The arrows indicate conductive
vessels. 3-7. Vitis riparia, native state. 3-8. C.
orbiculatus, after being flushed to remove embolism. 3-9. V.
riparia, flushed. Figures 3-10 to 3-13, stems collected on 18
June 1997. 3-10. C. orbiculatus, native state. The white
arrow indicates a conductive growth ring; the black arrow
indicates a nonconductive growth ring. 3-11. V; riparia,
native state. 3-12. C. orbiculatus, flushed. The white arrows
indicate conductive growth rings. 3-13. V; riparia, flushed.

47

 

48

 

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Figure 3-14. Frequency distributions of vessel
diameters (histograms) and percentage of total
theoretical kh(filled circles). (A) V: riparia (N = 333

vessels).
upon vessels from stems shown in Figures 3-6, 3—7,

3-10, and 3—11.

49

(B) C. orbiculatus (N = 356 vessels).

Based

:-:-:-:-: O M 355;; 2552 9
. . . .H. 'fi” W”" *I' ”f‘ I I
:3 <3 C) c:
<3 <3 C) E; E3 (q <3 \0 (D <3 (V ‘¢
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<3 C) <3 C> C) <3 :3 <3 c3 <3 C3
cu 3' ‘0 g; (3 0: Id \0 a> C) (V
H .—| I—I H H N N
50
B C. orbiculatus
4O _ $3123: N = 356
BOdéfifi
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-Efifii .H C) .’ ‘.
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on <3 0“ w! \0 «3 <3 cu
:4 PI .4 F1 <4 on N
vessel diameter (microns)

 

 

vulnerability curves were similar for C. orbiculatus and
V; riparia (Figure 3-15). From.the amount of scatter in the
data and the high amount of native embolism, it is difficult
to tell if there is any difference between the two species.
If there was a difference, C. orbiculatus was more vulnerable

to water—stress-induced embolism than V1 riparia.

Discussion

In Michigan, C. orbiculatus is considered an escaped
weed (Voss 1985). Its extensive and prolific growth suggests
that it possesses characteristics that set it apart from
native lianas. Apparently the sampled stems of C. orbiculatus
had significantly greater rates of secondary growth than V.
riparia since the stems of C. orbiculatus were, on average, a
half year younger (3.7 vs. 4.2 yr) but 8% wider than for V.
riparia.

Root pressure has been observed in many species (Sperry
et al. 1987; Ewers, Cochard, and Tyree 1997; Fisher et al.
1997) and may enhance conductivity by removing emboli. Root
pressure may also negate liana distribution limits imposed by
freezing—induced embolism. However, root pressure is
frequently too small to account for the elimination of emboli
in tall plants (Ewers, Cochard, and Tyree 1997). According to

my results, positive root pressures were mostly lacking in

50

 

 

 

 

E'T T 6 ,- " ,,,,,,,,,,,
. ”ir- ....... IL‘ """"
I -* - ------- I 1
.--' o
75‘ " l e.
5 T e I 11
'I'I A o."
.I , i I
O x’ .
g 50- " 1
0" 3
25-5
‘ y = 30.1LOG(x) + 74.6 0 V. riparia
y = 233mm") + 80-2 0 C. orbiculatus
O I I I
O ‘1 -2 -3 -4

xylem pressure (MPa)

Figure 3-15. Vulnerability curves. Each symbol
represents the mean for five segments from one stem.
Error bars represent +/— 1 SE. Where error bars are not
visible, they are smaller than the plotted symbol.

51

stem xylem of C. orbiculatus but present in V1 riparia; thus
they would not explain the weedy nature of C. orbiculatus.

The maximum.individual root pressure measurement of 145
kPa for V1 riparia found in this study would be sufficient,
in theory, to push water 14.5 m above the ground surface.
Other studies have reported root pressures for Vitis between
10 and 100 kPa (Sperry et al. 1987). Scholander, Love, and
Kanwisher (1955) reported sap pressures of 300 - 500 kPa in
Vitis labrusca. These measurements suggest that root pressure
is an important mechanism.for maintaining the conductivity of
xylem vessels in this genus. The vessels remained conductive
for up to 4 yr in the present study and up to 7 yr according
to Smart and Coombe (1983). In V1 riparia, increased embolism
coincides with the onset of freezing conditions. Apparently,
freeze-induced embolism.reduces transport capability, which,
in conjunction with defoliation induced by long nights,
brings about winter dormancy. Since the probability of
freeze-induced embolism increases with vessel diameter (Davis
et al. 1999), 100% embolism may not be achieved because the
narrower vessels in a stem.may not become air-filled. Greater
than 50% of the vessels in each species were narrower than 40
um.

The wood of C. orbiculatus is ring—porous, as compared
to the diffuse-porous wood of V; riparia, though the vessel

diameter distributions are similar and both are dependent on

52

wide vessels for most of their conductivity. Celastrus
orbiculatus appears to rely on the production of new wood to
re-establish conductivity instead of positive root pressure.
In 1997, percentage embolism in C. orbiculatus decreased
around the end of May, corresponding to the onset of
conductivity by new sapwood. This dependency of C.
orbiculatus on new wood production is similar to that
reported for temperate ring-porous trees (Wang, Ives, and
Lechowicz 1992; Sperry et al. 1994).

For both species the values of winter embolism were
essentially 100% for 1996, but often <100% for 1997. This may
be unexpected due to the different xylem anatomies of the two
species, but parallels the findings of Tognetti, Longobucco,
and Raschi (1998) who found the same trend looking at two
species of Quercus that differed in anatomy. The present
study may reflect the El Nifio weather patterns and the lack
of severe freezing during the winter of 1997-1998.

Vitis riparia had higher specific conductivity, both
initial and final, than C. orbiculatus. This is probably
explained by the fact that several growth rings were capable
of contributing to conductivity in the case of V; riparia,
but not for C. orbiculatus. However, using perfusion at high
pressure to remove emboli, additional growth rings may become
conductive in some cases. This may result in higher embolism

measurements by overestimating the maximum conductivity

53

possible. Thus the high native embolism reported here may be
due to refilling of permanently nonfunctional vessels,

especially for C. orbiculatus. Whether such embolism reversal
can ever occur in intact plants of C. orbiculatus is unclear.

Finally, the vulnerability to desiccation curves
indicate that both species are similar in their sensitivity
to drought—induced embolism“ Pawmmenter and Vander Willigen
(1998) point out that there are numerous models for analyzing
vulnerability curves. There is little agreement in the
literature as to statistical tests for vulnerability curves.
Our curve-fit approach represents the best fit available;
however, it does not reflect coefficients of biological
significance and should not be used to infer the native state
of embolism for these species. Importantly, it is not
possible to attribute the success of C. orbiculatus to
greater resistance to drought-induced embolism.

Clearly, the Vitis root pressure paradigm (Putz 1983,
Sperry et al. 1987) does not apply to all successful wide—
vesseled temperate vines. Celastrus orbiculatus has little or
no root pressure and is dependent on newly produced xylem
each year, similar to temperate ring-porous trees. The weedy
nature of C. orbiculatus cannot be explained by root pressure
nor exceptional conductivity. The results of this study
indicate that V; riparia has the advantage in the hydraulic

parameters measured, although it is possible that leaf or

54

root hydraulics, not measured in the present study, may favor
C. orbiculatus. However, there are many alternative
hypotheses not related to water relations that could explain
the reality of the C. orbiculatus spread. Among those
deserving attention are: the lack of pests and diseases
afflicting the exotic species, more prolific seed production
and dispersal, vegetative propagation from root sprouts, and

faster growth rates.

55

CHAPTER 4
Seed production and germination in the invasive liana
Cblastrus orbiculatus and the native C; scandens

(Celastraceae)

Introduction

Celastrus orbiculatus is a liana (woody vine) that is
native to Japan, Korea, and China. It has become a
problematic weed in eastern North America (Brizicky 1964,
Patterson 1974, Dreyer 1984, Tibbetts and Ewers 2000), and it
has been recognized as a threat to silviculture in the
Appalachians (McNab and Meeker 1987, McNab 1988). Damage to
host trees occurs from girdling, increased risk of ice
damage, and death from shading of the crown (McNab 1988). In
addition to silvicultural problems, exotic vines may impact
plant community dynamics, slowing or arresting succession and
replacing native vegetation (Penfound 1966). The native
congener, C. scandens, is less aggressive than C. orbiculatus
and can be supplanted by the exotic species when they co—
occur (Dreyer 1984). Manual removal of C. orbiculatus has
proven difficult due to resprouting from its extensive root
system; nonselective herbicides have had some success
following repeated exposures (Patterson 1974, Dreyer 1988,

Hutchinson 1992).

56

Morphologically, the two species are very similar. The
main difference used to distinguish the two is the
inflorescence: axillary cymes for C. orbiculatus and terminal
panicles for C. scandens. Both species are dioecious to
polygamodioecious. The gynoecium is usually 3 carpellate
(sometimes 4), 3-locular, with 2 (1) ovules per locule. The
fruit is a small (1 cm) orange to yellow subglobular leathery
capsule. It is incompletely 3-locular, 3 valved, with 2 (1)
seeds per locule. Seeds of both species have copious
endosperm, and 2n = 46 for each (Brizicky 1964, Gleason and
Cronquist 1991). The seeds are enclosed in a fleshy red aril
that is exposed upon reflexing of the valves in autumn. The
attractive fruits have been overcollected in Michigan leading
to the protection of C. scandens under Michigan Public Act
182 of 1962, the “Christmas—tree law" (Rabeler 1998). Both
species are also capable of vegetative propagation from root
sprouts, and birds disperse the seeds of both species. The
similarity in reproductive biology between the species stands
in contrast to their ecological behavior.

In Connecticut, Dreyer, Baird and Fickler (1987) found
that two populations of the exotic C. orbiculatus had higher
germination success (59% and 82%) than a population of the
native C. scandens (27%) in a laboratory study. Whether these
trends would hold true for Michigan, across several sites,

was unclear, as C. orbiculatus may be more recently

57

established in Michigan (Patterson 1974). Additionally, the
scarcity and small populations of C. scandens in Michigan
suggested that there may be some disruption or failure of its
sexual reproduction.

I hypothesized that C. orbiculatus would demonstrate
higher investment in sexual reproduction than C. scandens,
based on its demographic spread. This would be demonstrated
in greater number of seeds per fruit and greater seed

germination.

methods and Materials

Collection

Fruits were collected in the fall and winter of 1998—
1999 and 1999-2000 from six sites in the southern Lower
Peninsula of Michigan. Both species were collected on the
Michigan State University (MSU) campus and from nearby sites
in Williamston, Rose Lake, and Shoeman Road (Ingham county).
Celastrus orbiculatus was also collected from Kellogg
Biological Station (Kalamazoo county), and Hidden Lake
Gardens (Lenawee county). Fruits were randomly selected from
at least five individuals at each site, except where
population size was limiting (Rose Lake). The fruits were
allowed to air dry in the laboratory to make removal of the

fleshy aril simpler.

58

Processing

Seeds were separated from.the fruit. The number of
mature seeds per fruit was recorded for each species and
site. Seeds were weighed en masse, since they were too small
to accurately weigh individually, to obtain the mean mass per
seed. Finally, the seeds were stratified in screened sand in
plastic film.canisters at 5 °C for various periods of time.
Celastrus scandens seeds have a demonstrated stratification
requirement (USDA Forest Service, 1948) of 90 days at 33-50° F
(Barton 1939). Celastrus orbiculatus seeds were also found to
germinate better after a stratification period (Patterson
1974).

Subsamples of seeds were tested for viability using
2,3,5—triphenyl-2H-tetrazolium.chloride (TTC, 1%) (Mattson et
al. 1947, Castilla 1999). Seeds were imbibed in distilled
water, bisected through the embryo, and incubated in the

tetrazolium solution overnight. Viable embryos stained pink.

Germination

Germination trials were carried out in the laboratory.
Seeds of each species were sown in separate flats in Hyponex
Professional Mix Potting Soil. Seeds were planted
approximately 3 mm deep and watered throughout with distilled

water. No additional fertilizer or nutrient solutions were

59 f

introduced. Light was provided on a 12—hour cycle controlled
by electric timers. Light level was determined using an
Extech Instruments model 401025 light meter, the sensor of
which has its maximum sensivity at ~570 nm, range 400 to 700
nmt Light level, seed source, collection year, and
stratification period differed between trials. Table 4-1
outlines the conditions in each trial. Observations were made
roughly daily; the number of seeds germinated.was recorded. A
seed was considered to have germinated when its hypocotyl was
first observed. Subsequent death of a seedling was observed
on several occasions, this acted to slightly reduce the
percentage germination, as only live seedlings were counted
for each observation. In one trial (Trial 4) the seeds were
abraded with 100—C grit gypsum sandpaper to disrupt the seed

coat. The seeds were then planted as above.

Results and Discussion

Seeds per Fruit

The ovary anatomy indicates that both species had
similar potential reproductive output. However, this study
found significant differences in realized reproductive
output. Overall, C. orbiculatus had significantly more seeds
per fruit (3.68 i 0.05) than C. scandens. (2.43 i 0.07), with
P < 0.0001. However, when looking at individual sites this

trend was more variable (Figure 4-1). Based on population

60

 

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6
l MSU I MSU

.U 5" Rose Lake I KBS C
.,_| —
a 4_ E Shoeman Road E Hidden Lake d
IH b b
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(D
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C . scandens C. orbi cula tus

Figure 4—1. Mean seeds per fruit, +/— 1 SE. Sample sizes
are as follows: C. scandens at MSU N = 193, Rose Lake N
= 57, Shoeman Road N = 140; C. orbiculatus at MSU N =
312, KBS N = 336, Hidden Lake Gardens N = 355. Bars
designated with different letters are significantly
different from one another with P < 0.05.

62

means, Celastrus orbiculatus still produces more seeds per
fruit than C. scandens (2.9—4.4 vs. 2.3—3.0). However, fruits
of C. scandens collected at the Rose Lake site did not have
significantly fewer seeds than those fruits of C. orbiculatus
collected at the MSU site. This result quantifies the
anecdotal report of White and Bowden (1947) that both species
produce on average 3 to 4 seeds per fruit.

This study did not set out to specifically determine the
number of fruits per plant. To accurately compare this
parameter between species, it would be desirable to have
plants of equal age growing under similar conditions.
However, it was noted that C. orbiculatus plants generally
had more fruits per plant relative to similar sized C.
scandens plants. This was most likely due to a greater number
of shoots bearing fruits in C. orbiculatus than in C.
scandens. A post hoc analysis of shoots collected for the
seeds per fruit study indicated that individual fruiting
shoots of each species produced roughly similar numbers of
fruits: 14.4 in C. orbiculatus and 13.4 in C. scandéns. This
would suggest that any advantage to C. orbiculatus would
occur from.producing more fruiting shoots, with fruits that

bear more seeds per fruit than C. scandens.

63

Seed Haas

While being more numerous, C. orbiculatus seeds were of
consistently lower mass than seeds of C. scandens (Figure 4-
2). Mean seed mass across sites for C. orbiculatus was 10.3 i
1.1 (SE) mg, while for C. scandens mean seed mass was 16.8 i
0.4 mg. An unpaired t-test shows these differences are
significant (P = 0.0055). This would indicate that seeds of
C. orbiculatus would have less of the copious endosperm
reported for both species than C. scandens. (Gleason and
Cronquist 1991). Relative to one another, C. orbiculatus
would be considered more r—selected and C. scandens more K-
selected based on this character (MacArthur and Wilson 1967,
Pianka 1970). This result is not likely to represent an
aberrant year; C. scandens is reported to bear good seed
crops almost yearly (USDA 1948), and is not prone to masting

(WYman 1950).

Seed Viability

The differences in seed viability between species were
minor. Staining for vital tissues using TTC indicated that
88% (n = 140) of C. orbiculatus seeds were viable versus 79%
(n = 138) for C. scandens. Floatation was not a good
indicator of the absence of a viable embryo in C. scandens:
40% of floating seeds contained viable embryos versus 100% in

C. orbiculatus. However, 95.7% of sinking C. scandens seeds

64

 

 

 

 

 

 

30
I MSU I MSU

’5, Rose Lake I KBS
E
V I Shoeman Road I Williamston
W3 20-
Q)
Q)
m
kl
Q)
Q. 10—1
0)
3
E

0..

 

C. scandens C. orbi cula tus

Figure 4-2. Mass per seed. Sample sizes are as
follows: C. scandens at MSU N = 453, Rose Lake N =
234, Shoeman Road N = 376; C. orbiculatus at MSU N =
291, KBS N'= 236, Williamston N = 624. Seeds were
weighed en masse, so SE could not be calculated.

65

did have embryos, indicating that screening for sinking

should yield potentially viable seeds.

Germination

The germination trials revealed a striking difference
between the germination success of the two species (Figure 4-
3). In each case the seeds of C. orbiculatus were more likely
to germinate under controlled laboratory conditions than the
seeds of C. scandens. The percentage germination ranged from
45 to 92% for C. orbiculatus and from 0 to 1.5% for C.
scandens. Germination began one week following sowing and was
largely complete by three weeks. Trial four was followed for
129 days with no increase in number of seeds of either
species germinating.

The higher success of C. orbiculatus seeds to germinate
was not surprising, as others have noted similar results
(Dreyer Baird and Fickler 1987). The germination success for
C. orbiculatus appears to be in line with reported
germination capacities for other temperate lianas
(Parthenocissus quinquefblia, 69%; Vitis riparia, 82%; USDA
Forest Service 1948). However, the extremely low success of
C. scandens seeds to germinate, always below 2%, was
surprising. The USDA Forest Service (1948) reported a mean
germination success of 47%, ranging from 9 to 80% for this

species. Dreyer, Baird and Fickler (1987) found germination

66

 

100 —0— Trial]

”do
-- -__ _____.-
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, i , 'I
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I l" I I --- - > ........
O :-:o:-:6..£0.:.0.f321fotl?ow:30:?wo.‘o:‘.on‘.
O 10 20 3O 40

day since planted

Figure 4-3. Germination trials. Open symbols for C.
scandens, closed symbols for C. orbiculatus. See Table
4-1 for the conditions of each separate trial.

67

 

rates of 27%, and Joseph (1928) reported 36 to 68%
germination. All of these earlier studies used similar cold
stratification periods, light levels, and soil types to the
methods implemented here.

Though these seed germination results do help explain
the observed pattern of C. orbiculatus spread relative to C.
scandens, they also beg the question: Why did the C. scandens
seeds fail to germinate? Seed scarification was investigated,
although it had not been reported as a necessary prerequisite
for germination. The same results were obtained when the seed
coats had been disrupted, so it is unlikely that this
explains the low germination success of C. scandens.
Likewise, the same results were found for seeds from
different sites and from seeds collected in both 1998 and
1999.

I do not have a clear explanation of the low germination
success of C. scandens in this study. Some reports (e.g.,
USDA 1948, White and Bowden 1947) indicate that good seed
years are experienced almost annually, others (wyman 1950)
indicate that year to year trends exist and can be
significant. In this light, it is possible that I have
documented two bad years for C. scandens. However, it seems
unlikely that two bad years for one species would prove to be

relatively good years for a sympatric congener which might be

68

expected to cueing on the same environmental parameters for
seed production.

One possible hypothesis is that C. scandens is suffering
from.inbreeding depression. A normally outcrossing species
may suffer from.inbreeding depression when in small, isolated
populations (Barrett and Husband 1990, Husband and Schemske
1996). Modeling has indicated the possibility for moderate
amounts of selfing to lead to high inbreeding depression
(Lande et al. 1994). unfortunately, I have no information on
population structure, demographics, or the frequency of
selfing in C. scandens or C. orbiculatus.

Alternatively, populations of C. scandens may be
suffering from an accumulation of deleterious somatic
'mutations. With reduced numbers of sexual generations through
time, C. scandens would have fewer chances for selection to
operate, purging deleterious alleles. This could eventually
result in poor vigor and loss in realized sexual reproductive
success (Kondrashov 1994).

Grime (1979) life history strategies would characterize
both species as ruderals. One would expect that the large
seeds with abundant resources should.promote a high
germination rate for C. scandens. Conversely, one would
expect the many small seeds of C. orbiculatus, with limited
resources, would demonstrate a low germination rate. This

would be particularly true under field conditions, and less

69

apparent in the laboratory. No such failure in C. orbiculatus
or advantage to C. scandens seeds was observed in this study;
C. orbiculatus is more successful as a ruderal in Michigan.
While this study found a distinct difference between the
species in seed germination, it did not investigate seedling
establishment or seedling survival. Differences in these
characteristics could strongly enhance or negate the
germination success measured in the laboratory. Additionally,
both species are capable of persistence and spread by
vegetative means. Whether the two species differ in this
capacity was not specifically investigated, and could

similarly affect the results reported here.

Predictive Theory

Much work (see Rejmanek 1996) has focused on elucidating
the traits of invasive species in order to successfully
predict which species will become pests. This could have
direct management implications regarding which species are
introduced through horticulture and agriculture. Rejmanek and
Richardson (1996) developed a discriminant function based on
three traits that differed between invasive and non—invasive
pines: low seed mass, short juvenile period, and short
interval between large seed crops. Bird dispersal of seeds
also contributes positively to the invasiveness of a species

(Rejmanek 1996). The discriminant function correctly

70

identified the invasive lianas Lonicera japonica and Pueraria
lobata (Rejmanek and Richardson 1996). Although the length of
juvenile period has yet to be determined for C. orbiculatus,
low seed mass, near yearly good seed crops, and bird
dispersal of seeds indicate that it follows well with this

predictive function for invasive species.

71

CHAPTERS
Growth, phenoloqyy and herbivory in Cblastru: orbiculatus and

Vitis riparia

Introduction

The invasive liana (woody vine) Celastrus orbiculatus is
spreading through habitats that have native incumbent lianas
including Vitis riparia, Parthenocissus quinquefolia,
Toxicodendron radicans and C. scandens. While C. orbiculatus
was first introduced around 1900, its localized spread into
suitable habitat continues (Chapter 2). Possible explanations
for the spread of an alien species into occupied habitat are
enhanced growth and lower incidence of herbivory relative to
the native species. Some exotic lianas (e.g., kudzu, Forseth
and Teramura 1987) exhibit higher growth rates than competing
vegetation. Other exotic lianas appear to benefit from
escape from.herbivory as proposed.by Darwin (1859); for
instance, Lonicera japonica (Schierenbeck et al. 1994).

Shoot growth is a major way by which plants expand their
canopies and explore their light environment. This is
especially important in lianas, where the relative amount of
leaf area supplied per stem section is high (low Huber
values). Liana growth rates may be enhanced since fewer
resources need to be allocated to supporting stem tissue

(Mooney and Gartner 1991).

72

Any damage to the liana stem.may have growth
consequences within the stem and within the whole plant. Loss
of the shoot apical meristem may lead to lateral buds
proliferating to replace it (Kramer and Kozlowski 1979). The
loss of apical dominance may also lead to changes in the
allocation of elongation between shoots (Collet, Colin and
Bernier 1997).

Direct loss of leaves can also affect shoot growth. Both
the position and extent of leaf loss can affect shoot
elongation (Marquis 1988, 1992, Tuomi et al. 1988, Haukioja
et al. 1990, Langstrom et a1. 1990, Henriksson, Haukioja and
Ruohomaki 1999). Additionally, timing of leaf loss can
determine the extent of shoot growth response (Haukioja et
al. 1990, Ruohomaki et al. 1997).

The precocious internode elongation of lianas may make
their apices more susceptible to herbivory than plants with
protected apices (Penalosa 1983). Additionally, tendril
climbers such as V: riparia should have less exposed apices
relative to twiners like C. orbiculatus (Troll 1937). There
is evidence that apex predation may limit population
survivorship in some vine species. Janzen (1971) found severe
herbivory on the apices of Dioclea megacarpa (Fabaceae),
ranging from 15 to 50% of shoot tips.

The recent spread of Celastrus orbiculatus throughout

lower Michigan suggests that it may be growing unchecked by

73

predators that hamper native lianas. There are very limited
reports of herbivory on C. orbiculatus either in its native
range (Saito 1989) or in Michigan (Kiss 1984). The native
congener, C. scandens (American bittersweet), is reported to
suffer severe winter injury from cottontail rabbit (Sweetman
1944). Herbivory on Vitis is well documented through
viticulture, and includes insects (Phylloxera sp., root
louse; Erythroneura vaiabilis, variegated leafhopper; and
Harrisina brillians, western grapeleaf skeletonizer) and
nematodes (Meloidogyne, Pratylenchus, and Tylenchulus)
(Mullins, Bouquet and Williams 1992).

I wished to determine whether the spread of C.
orbiculatus was related to a lack of herbivory, greater shoot
growth, or a combination of both, relative to the common

native liana species Vitis riparia.

methods and.Materiels

Thirty-four species pairs of individuals of Celastrus
orbiculatus Thunb. and Vitis riparia Michaux were established
in the natural regrowth forests surrounding Kellogg
Biological Station, Michigan State University, Gull Lake,
Michigan in 1998. One new season's shoot of each species was
marked with flagging tape. The shoots were selected to be as
close to one another as possible, as similar in size as

possible, and experiencing the same microhabitat influences

74

as could be discerned (e.g., same level in canopy or at
ground level). Individuals were located in varying habitats,
including open fields, closed canopy deciduous forest, and
edges.

In 1999, thirty-seven species pairs were used. New
shoots on the same stems used in 1998 were used for
measurements in 1999. Several were dead and were eliminated
from the subsequent year.

Measurements were made through the 1998 and 1999 growing
seasons. Shoot length and leaf size at the third node were
measured weekly until no change was detected. Phenological
parameters of bud burst, leaf maturation, and leaf fall were
monitored. Across sites, average date of leaf maturation,
full shoot extension growth, and average maximum.shoot length
were calculated. The maximum shoot length reflected the
greatest amount of growth recorded during the growing season,
which was not necessarily the shoot length at the end of the
season. Frequency of deer and insect herbivory, as well as
likelihood of mortality, were calculated. Notes on damage by
both deer and insect herbivores were made, and resprouts were
followed when herbivore damage removed the initial shoot.
Light level was measured with an Extech Instruments model
401025 light meter (peak sensitivity ~570 nm, range 400—700
nm) in 1999 to compare the sites. Means were compared with

two-tailed t-tests, alpha = 0.05.

75

Results

Mean maximum.shoot length differed between years, but
was relatively similar in both species, and reached by the
same time in the growing season (Table 5—1). Shoots in low
light grew longer than shoots in high light (Figure 5-1).
Leaf maturation was complete slightly earlier and leaf drop
occurred slightly later in C. orbiculatus than in V3 riparia
in both years. Bud burst, observed in 1999, occurred slightly
earlier in C. orbiculatus (128.1 : 1.0) than in V1 riparia
(130.1 i 1.2). Flowering, observed in 1998, occurred slightly
earlier in C. orbiculatus (142 i 0) than in V1 riparia (145.8
i 1.5). Overall, there was very little difference in the
timing of phenological events between the two species.

Overall mortality of shoots was greater for V1 riparia
than C. orbiculatus in both years, but incidence of herbivory
differed between species and between years (Table 5-2). In
1998, V1 riparia was slightly more likely to be eaten by deer
than C. orbiculatus (50 vs. 44%). However, C. orbiculatus was
slightly more likely to be eaten by insects than V; riparia
(82 vs. 79%). In 1999, V1 riparia was much more likely to
suffer deer browsing than C. orbiculatus (70 vs. 30%).
Contrary to 1998, in 1999 V2 riparia was much more prone to
insect predation than C. orbiculatus (30 vs. 14%).

The consequences of herbivory, while correlational,

suggest both species and year differences do exist. In 1998,

76

 

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77

150

 

 

 

 

 

 

B
125‘
100-
E
L)
V7S—d
.C:
‘5»
50‘
:1
G)
H
25‘
O I l l l l I
MAY JUN JUL AUG SEP OCT
_._ 10W light ........ O ........ high light
C. orbiculatus C. orbiculatus
+ 10W light ........ D ........ high light
V. riparia V. riparia
75
B

L
‘,

 

 

 

E
.. /. ................... ...
u ..... I ......... I ................. I .......................................
., g ............... . ................. , .........
a“, ...........
H II- _ ”-2.
* O
O I [ 1 I l I
MAY JUN JUL AUG SEP OCT
date

Figure 5-1. Mean shoot length, +/- 1 SE. (A) 1998. (B)

1999. Low light level < 1000 lux, high light level >
1000 lux.

78

most C. orbiculatus shoot mortality was associated with
insect herbivory, while shoot mortality in V; riparia was
associated with deer herbivory, insect and deer herbivory
combined, and to a lesser extent insect herbivory alone
(Figure 5—2). In 1999, most shoot mortality in both species
was not associated with any observed evidence of herbivory.
Deer herbivory and combined deer and insect herbivory were

associated with equal portions of V; riparia shoot mortality.

Discussion

Celastrus orbiculatus and V1 riparia were very similar
in phenology and shoot elongation in this study. This is
particularly interesting as they are from different plant
families and climb by different strategies (V1 riparia a
tendril climber, C. orbiculatus a twiner). Timing of
phenological events and overall maximum shoot elongation
differed by year, but not by species. These trends are
consistent with our previous experience at a different site
in Michigan (Tibbetts and Ewers 2000). The year to year
trends are likely related to differences in summer
precipitation and temperature (Figures 5-3 and 5—4). The
similarity in species responses appears to indicate that the
selective pressures relative to the liana growth habit are

stronger than family-specific trends.

79

 

 

 

 

 

     

40
>‘ 1998 1999
.3.)
-:-|
H 30- deer
m
I: insect
O deer + insect
55 20-
4a) unknown
8
L. 10-
(D
Q.

I
~ 0
.y
.Q’b‘
£3 $8
. 0'6
0' 0'

Figure 5—2. Sources of mortality, 1998 and 1999.
Note that the total mortality was greater in V.
riparia both years (see Table 5-2).

80

 

 

 

 

 

1998

"150-
c:
C)
'3
(U 100"
J.)
-r-l
CL
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Q)
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C)
-.-|
‘3 100-
l.)
"-1
9:
() 50‘
G)
Ll
CL

0

JAN FEBMAR APR MAY JUN JUL AUG SEP OCT NOV DEC

Figure 5-3. Precipitation. 1998 and 1999 monthly
totals from.the Kellogg Biological Station Long Term
Ecological Research site weather station.

month

81

 

 

 

 

 

 

 

30
1998
204
Q
10-
0 /
-10
1999

20‘

mean monthly temperature
to
O

10"

 

0/

 

 

 

—10
JAN FEB MAR APR MAY JUN JUL AUG SEP OCT NOV DEC

month

Figure 5-4. Temperature. 1998 and 1999 mean monthly
temperature from the Kellogg Biological Station Long
Term Ecological Research site weather station.

82

Herbivory damage was similar on both species in 1998,
but in 1999 V; riparia was much more likely to show signs of
herbivory. This may be related to a combination of factors.
The lower overall shoot elongation seen in both species in
1999 may have resulted from lower precipitation levels than
1998 (Figure 5-3). If herbivore density in 1998 and 1999 was
similar, one would expect to see greater herbivory in the
year with less growth, since there would be less biomass
available to the herbivores. Additionally, many herbivores
may not recognize the exotic C. orbiculatus as a potential
food item" Finally, it may be possible that V: riparia lacks
secondary defenses while C. orbiculatus has such defenses.

Mortality of shoots differed between species in both
years, suggesting that V: riparia suffers higher shoot
mortality than C. orbiculatus. The shoot mortality difference
between species also suggests a difference in shoot growth
strategy. Damaged Vitis riparia shoots were likely to be
replaced with a new sprout from.the base rather than to
continue growing from a lateral bud. In 1999, eleven damaged
shoots were replaced by resprouts in V3 riparia, with one
shoot being replaced three times. In contrast, C. orbiculatus
shoots that suffered damage were likely to continue growing
from a released lateral bud.

The difference in shoot response to injury may relate to

differences in stem.architecture. Vitis riparia shoots

83

typically had fewer, larger leaves relative to C. orbiculatus
shoots. The best response to injury to V3 riparia stems
coupled with leaf damage, indicating a risky environment, may
be to try a new environment. However, when in a productive
environment, V2 riparia produced numerous lateral branches (2
= 4.6 1 1.0 per stem vs. 0.8 i 0.3 for C. orbiculatus, 1998).
Ce1astrus orbiculatus shoots continued to elongate from
lateral buds. This was further demonstrated in an simulation
of herbivory in the laboratory. Eighty-four four month old C.
orbiculatus seedlings, ranging in height from 7 to 50 cm,
were cut back to 5 cm.with blunt scissors, simulating
herbivory. Ninety-five percent of the seedlings resprouted
from lateral buds and continued to grow.

While C. orbiculatus does not entirely escape herbivory,
it may suffer reduced rates and respond vigorously. This may
be enough to explain its advantage over V2 riparia in this
study. Additionally, the reduced herbivory effect on C.
orbiculatus may also explain its spread relative to the

native congener C. scandens.

84

CHAPTERS
Dendrochronology applied to the exotic temperate liana

Cblastrus orbiculatus

Introduction

Dendrochronology has typically been applied to tree
species. However, the principles extend to any species having
secondary growth with boundaries between growth increments,
relatively concentric growth rings that show variability in
patterns, and cross-dating within and between individuals. A
multitude of species meet these requirements including, as
one would expect, most temperate trees (e.g., Fritts 1976,
Graumlich 1993). Non-tree species have also been examined,
such as the herbaceous perennial Bunias orientalis L. (Dietz
and Ullmann 1998). Additionally, both tree species and fish
have been shown to have annual growth increments correlated
to climate variables (Guyette and Rabeni 1995).

Many lianas (woody vines) have the required
characteristics for dendrochronology. However, the
dendrochronological literature is lacking in studies of liana
growth rings. Only one dendrochronology study includes any
aspect of liana growth. Birrong and Schoenwiese (1988)
carried out a climatic study using European tree rings. At
one site, they used the quality of grape harvest instead of

tree growth as a proxy for climatic data. The growth rings of

85

the grapevines were not evaluated. One reason for the paucity
of liana dendrochronology may be the relatively short life
span of lianas compared to trees. However, this shortfall may
be countered by cross-dating overlapping chronologies.
Dendrochronology has been used to examine the effects of
exotic species on community composition and dynamics (Russian
olive and salt cedar: Howe and Knopf 1991, exotic deer:
veblen et al. 1989), to determine the establishment time of
invasive trees (Butler 1986, Miller and Halpern 1998).
Celastrus orbiculatus is an exotic liana pest species in
Michigan (Patterson 1974). It was desirable to understand its
history at several sites, and how its growth compares to a
native co-occurring liana, Vitis riparia. The objectives of
this study were: 1) to determine if the lianas C. orbiculatus
and V3 riparia could be used in dendrochronology, 2) to
compare annual growth increments (ring widths) in C.
orbiculatus and V2 riparia with precipitation data, and 3),
to determine the relative age and dynamics of C. orbiculatus

infestations at three different sites.

methods and materials
Vines were sampled at the Petrides farm, Hidden Lake
Gardens (HLG), and the Kellogg Biological Station (KBS). Each
site was chosen based on the presence of large populations of

the exotic liana C. orbiculatus and some specimens of V.

86

riparia. The site location details and sample sizes are
presented in Table 6-1. Each site was examined for C.
orbiculatus specimens: all those greater than 5 cm in
diameter were sampled. Stem segments were cut in the field as
close to the proximal base as possible and returned to the
laboratory for drying and analysis. Specimens collected
included dead and apparently living stem sections
approximately 20 cm in length.

Upon return to the laboratory, the stems were cut to
yield discs approximately 3 cm thick. The discs were dried in
a 60 °C oven for two days. Surfacing was carried out using
sand paper. Chronologies were created using the skeleton
plotting technique (Stokes and Smiley 1996). In this
technique, representations of the narrow ring widths for each
stem are made on strips of graph paper. The individual
chronologies can then be compared by overlaying the graph
paper strips and matching the patterns of narrow rings.
Skeleton plotting was done using a dissecting microscope. Two
chronologies, 180° degrees apart, were completed for each
stem“ This allowed me to verify consistent patterns within
the stem (internal cross—dating). Stems that were alive at
the time of sampling provided an anchor date to assign dates
to dead stems. A master chronology for each species at each
site was made by matching ring width patterns and extending

the record back as far as the oldest stems.

87

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88

Ring width measurements were made with a Henson
measuring machine. This device records the width of each
growth ring in increments of 0.01 mm. Two series of
measurements were made for each stem, 180° degrees apart, to
calculate the mean ring width. The ring width chronologies
were then aligned by year to calculate mean ring width for
each species at each site.

Precipitation data for the period 1950-1999 were
obtained from.the NOAA weather web site (www.noaa.gov). The
nearest weather stations with continuous, relatively complete
records were utilized as indicated in Table 6-1. Missing
values were inferred from the nearest station to provide a
continuous record. Stem.chronologies were aligned and ring
widths were compared with precipitation data in a correlation

analysis.

Results

Celastrus orbiculatus and V1 riparia were found to
produce reliable, reproducible ring width patterns. Cross-
dating was achieved. Additionally, locally absent (missing)
rings were noted in both species, indicating that simple
ring-counting would not have produced reliable results.

Representative ring width chronologies are shown in
Figures 6-1, 6-2 and 6—3. Both species demonstrate internal

consistency, with the ring width chronologies 180° apart from

89

 

1200

(mm)

1000-

ion

tat
<p
<3
?

Cl

C

O
l

preC1p1

 

 

lb
0
O

 

300

250-

200‘

150-

dth (0.01 mm)

ring W1

100‘

l

50

 

 

 

1975

1980*
1985-
1990‘

year

Figure 6-1. Aw Annual precipitation at Petrides
farm” B. C. orbiculatus ring width chronology. The
separate lines represent two chronologies for the
same individual.

90

 

1995

 

 

 

 

 

 

 

 

 

 

 

 

 

 

’E A

1000*

I:

C)

'3

(58004

I.)

-I-i

3' U

0600-

Q)

3..

CL

400 I I I I

z~d250

E B C. orbiculatus

r4 9

0.200‘ s

e g - .

150- .-. ° . . -° §

3‘3 ’ . V ’5.

I'd E '-.. . I. ."

-H .0. fl 0 ..."-.

31001 .0" "9; ,9. 5.9.. .

E3? = . 6

'1". . . . 0.. .2. . v

H 50 l l l I .
c> CD C3 C” C) CD
Ln \0 l\ (I) 0‘ O
m m 0‘ m m o
H H H H v—I N

year

Figure 6-2. A. Annual precipitation at Kellogg
Biological Station. B. C. orbiculatus ring width
trend. The separate lines represent two chronologies
for the same individual.

91

 

 

 

 

 

 

 

 

 

 

 

 

 

 

A1200
E .A
10003

C!

C)

'3

(U 800-

J.)

'3.

'r-I 600‘

8

LI

0.. 400 I I I I

250 o I

E B I

F4 200‘

CD

51150-

A:

g 1001

-<-l

3

m 50"

E

’4 o I . . .
C) c: c: c> c> <3
U) \o r~ an ax <3
ox ox ox ox ox <3
V4 r4 r4 r4 <H cu

year

Figure 6-3. A. Annual precipitation at Kellogg
Biological Station. B. V; riparia ring width trend. The
separate lines represent two chronologies for the same
individual.

92

the same individual matching one another relatively closely.
The annual growth rings correlate with some periods of the
precipitation record, but do not precisely match.
Additionally, individuals of the same species at the same
site show some consistency in mean ring width chronologies.
Celastrus orbiculatus and V1 riparia at KBS show consistent
patterns of valleys and to a lesser extent peaks (Figures 6-4
and 6-5).

Mean annual ring width plots showed similar tracking of
the precipitation record. At the Petrides farm (Figure 6-6),
the peak at 1986 in growth ring width and the following
valley in 1988 corresponded to the high precipitation in 1986
followed by the drought in 1988. Vines of both C. orbiculatus
and V1 riparia at KBS (Figure 6-7) showed a similar tracking
of precipitation patterns. The responses of both species were
very similar to one another throughout most of the
chronology, though C. orbiculatus possessed wider growth
rings during the decade 1989—1999. At HLG, a rough tracking
of precipitation pattern was also observed (Figure 6—8). The
mean ring width of C. orbiculatus increased throughout the
chronology, from.heing narrower than V; riparia in the 1970’s
to wider in the 1990’s.

While the general patterns suggest that mean annual ring
‘width appears to be associated with precipitation, a

correlation analysis failed to find strong positive

93

ring w1

 

250
200‘
150—
100-

50‘

 

 

 

 

250
200*

150—

(0.01 mm)

100-

dth

50‘

 

 

 

 

250
200—
150‘
100*

50—

 

 

 

1950

1960-
1970-
1980-
1990-

year

Figure 6-4. Ring width chronologies for C. orbiculatus
at KBS. Each plot represents the mean ring width
chronology for one individual. Note the consistent
valley at 1979.

94

2000

 

250
200-
150-
100-

50-

 

 

 

 

250
200-
150-
100‘

50—

 

 

 

250

ring width (0.01 mm)

200‘
1501
100‘

50‘

 

 

1950

1960—
1970*
1980-
1990-

YEEEE
Figure 6-5. Ring width chronologies for V1 riparia at

KBS. Each plot represents the mean ring width for one
individual. Note the consistent valley at 1974.

95

 

2000

 

1100

O

O

O
l

tation (mm)

prec1p1

ON \‘I oo \0
O O O O
O O O O
l J l J

 

 

 

500

 

250

2004

dth (0.01 mm)
H
U1
C.”

 

_O_

 

C. orbiculatus

 

 

100-
«4
3

U) 50-
C
-H
H

0

c>

[\

ox

PI

1975-

19804

1985-

year

1990-
1995-

Figure 6-6. A. Annual precipitation at Petrides farm.

B. Mean ring width of C. orbiculatus,

96

+/- 1 SE.

 

2000

 

1200

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

A A
\’1000‘
c A
C)
'l‘l
.IJ
8
W4 800-
Q-l
"—4
L)
m v
¥I
‘1' 600-
200
B
E I TT f T _.
150* ’ vA I. h 0. 00‘!“ T
H .17 ' O ”‘Q‘yl . .L ‘T.T
O :z T T . "O :1... .L ._L r.
. 1 TT 1‘5 3‘E52 1 .L
3 1 TT °"§'1'?IT,.
rd :‘0 “'l TU-I T J- .:..
:3 ., ‘11:“ 'I
.H o . . o. ‘g '.\‘L .L
3 * J 1 H
50‘
CD
El —0— C. orbiculatus
¥l
........ ......... V. r i p a ria
0 I I ' I
O o O O O 0
L0 to l\ (D ON 0
m m ON ON Ch O
H H H H H N

year

Figure 6—7. A. Annual precipitation at Kellogg
Biological Station. B. Mean ring width, +/- 1 SE.

97

 

1000

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

”5900- A

8.8001
'r-I
.1.)

S
-H 7004
D:
-H

8
L1600‘

04

50C) . I I T
.200
—°— C. orbiculatus

E ........ . ........ V. riparia
o T ‘.°.

‘ T TTT .: I ‘ fTT
0 Ti 9 TT ‘ '5 0.0
V aTTg'qn-Jq 1

100‘ i‘T. .- ' 'fl";£ =.
PG - ”I: .1. 0|; T'T T
‘J 11"T*-- MTTMT
'3 T .7? ~ iris-
3 T T O .L .L
50" ii. A
CD ' .
C:
-r-|
Fl
0 1 I I I
O O o O O O
m \0 b m m 0
ox m m 0 Ch 0
H H H H H N
)NEEEK

Figure 6-8. A. Annual precipitation at Hidden Lake
Gardens. B. Ring width, +/- 1 SE.

98

relationships with various components of summer precipitation
(Table 6-2). The current year’s ring width of C. orbiculatus
was slightly positively correlated with most parameters of
precipitation, particularly at HLG. Vitis riparia current
year’s ring widths were not generally positively correlated
with precipitation. The influence precipitation on the
following year’s ring width roughly followed the same trend
for each species. However, at KBS, ring width of the V.
riparia was positively correlated with precipitation.
Establishment dates for C. orbiculatus at each site,
along with vine lifespan suggest dates by which each site was
invaded. Petrides farm.was invaded by the early 1970’s, with
many vines living until sampled (Figure 6-9). Numerous vines
at Petrides farm.died around 1996. This time corresponds to a
massive manual eradication effort, carried out by cutting
many vines. HLG was strongly invaded in the mid—1970’s, with
all vines living until sampled (Figure 6-10). KBS was invaded
earliest, with a living vine found that was established.by
1952 (Figure 6—11). Most of the vines sampled at KBS were
still living at the time of collection. At each site,
establishment of C. orbiculatus appears more clumped in time

than for V1 riparia.

99

 

 

 

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100

 

 

V3 riparia

 

 

 

 

 

C. orbiculatus

 

 

 

 

 

 

 

 

 

 

 

 

 

 

l I l l

O O O O 0

Ln KO 1‘ co m

m Ch ON m m

H H H H H
year

Figure 6-9. Lifespan of vines sampled at Petrides
farm” Each horizontal represents one individual.

101

 

2000

 

 

 

‘V. riparia

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

C. orbiculatus

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Figure 6-10. Lifespan of vines sampled at Hidden
Lake Gardens. Each horizontal line represents one
individual.

102

 

l I I I
'O O O O O 0
Ln KO l\ co Ch 0
m m Ch m Ch O
H H H H H N
year

 

 

 

V. riparia

 

 

 

 

 

 

 

 

 

 

 

 

C. orbiculatus

 

 

 

 

 

 

 

 

 

 

 

 

 

I I I I

O O O O 0

Ln \0 l‘ 00 ON

Ch Ch m ox m

H H H H H
year

Figure 6—11. Lifespan of vines sampled at Kellogg
Biological Station. Each horizontal line represents
one individual.

103

 

2000

Discussion

This study demonstrates that temperate lianas may serve
as reasonable dendrochronological study species. Both C.
orbiculatus and V1 riparia provided cross—dated chronologies
that were internally consistent for individuals.
Additionally, chronologies cross—dated between individuals of
the same species at the same site, though they were not
perfectly aligned as indicated by noise around the trend
lines. This likely represents individual variation in
physiology and differential sensitivity to climate.
Chronologies for each species at the same sites differed
slightly, indicating that there may be species—specific
differences in responses to climate. Locally absent rings
were discovered in both species, indicating that simplistic
ring—counting would not have been effective.

The oldest C. orbiculatus specimens were still living.
The fact that dead.material was not older raises two points.
First, the young age of much of the material makes it
difficult to be certain of the dating. With only a few points
to work with, there are several possible dates that match the
pattern. Those dates assigned in this study were subjectively
the most parsimonious. Second, the ring—porous wood anatomy
of C. orbiculatus and the fact that lianas generally provide
little of their own mechanical support (hence few fibers) may

mean that the dead liana debris decomposes rapidly. Thus,

104

older material may have existed at some point in time, but is
currently unavailable through loss to decomposition. This
possibility is supported by the difficulty in surfacing some
of the discs from dead samples, where the wood was too soft.

The apparent correspondence between chronologies and
precipitation did not prove significant or consistent through
correlation analysis, either the present year’s precipitation
or the previous year’s precipitation. While precipitation is
a major determdnant of plant growth, it is not the only, and
may have been outweighed by some other factor. Additionally,
if a more discrete measure of precipitation, such as winter
snowfall and consequent meltoff, was the most important, that
detail would have been missed in this analysis.

The difficulty in obtaining a good, continuous climate
data set reasonably close to each site is a serious problem
that may hamper the detection of such relationships. However,
it is important to acknowledge that spurious significant
results may be detected if enough details are examined.
Additionally, this study has not explicitly examined
potential effects of juvenility. Strategies are available for
removing juvenile growth trends in trees; however, no such
strategies are available for lianas.

While the trends of ring width and precipitation have
not proven significant, the chronologies themselves offer

several insights into the establishment and invasion of C.

105

orbiculatus. Dendrochronology effectively indicates the date
by which each site was invaded by C. orbiculatus. At both HLG
and KBS, the ring widths of C. orbiculatus are initially
narrower than those of V1 riparia, but by the 1990’s they
were consistently wider. This may indicate that C.
orbiculatus is enjoying a growth advantage over V1 riparia.
It may also represent an advantage of V3 riparia over C.
orbiculatus, since V1 riparia may reuse xylem.for
conductivity through root pressure but C. orbiculatus does
not. This has earlier been shown in the larger, younger stems
of C. orbiculatus relative to V3 riparia stems analyzed for
hydraulic conductivity (Chapter 3).

The clumping pattern of C. orbiculatus establishment
times suggests rapid recruitment of individuals. The long C.
orbiculatus chronologies, (max. = 47 years, KBS),
demonstrates that individuals may be long lived providing
ample time for both vegetative spread and seed dispersal.
Additionally, the fact that most C. orbiculatus individuals
were living at the time of sampling indicates that the
spread of C. orbiculatus will continue to be a serious
problem in all of these sites.

Finally, it appears that of these three sites, the
invasion of C. orbiculatus first occurred at KBS. It is
possible that the bird sanctuary adjoining KBS was the source

of introduction, either indirectly from migrating birds, or

106

directly by wildlife managers at the sanctuary. There is no
direct evidence of planting C. orbiculatus at the sanctuary,
though some previous managers were fond of other exotic
wildlife forage species. Hidden Lake Gardens and the Petrides
farm have been invaded relatively recently by C. orbiculatus.
This may indicate that C. orbiculatus is still spreading in a

northward direction throughout the state.

107

CHAPTER?

General Conclusions

The exotic liana celastrus orbiculatus appears to thrive
in Michigan for reasons understood as long ago as Darwin
(1859): absence of effective predators in the form of
herbivores and competitors in the form of other plant species
with the same niche. Since Darwin, the characterization of
species following r- or K-selected life history strategies
also defines traits associated with successful invaders.
Techniques such as dendrochronology provide a means of
tracking and understanding invasion patterns.

Contrary to being “invisible” to herbivores, C.
orbiculatus does suffer from.herbivory. The effects of both
insect and deer herbivory were observed on C. orbiculatus.
However, its response to herbivory differs from the common
native species Vitis riparia. In V2 riparia, herbivory
frequently translated into shoot mortality, but this was not
the case in C. orbiculatus. While herbivory was greater on V;
riparia in a year of relatively poor shoot elongation growth
(1999), V; riparia did not suffer higher shoot mortality.

Competition from native lianas does not appear to affect
C. orbiculatus. This may suggest that the liana growth habit

is underrepresented in the Michigan flora, and that the niche

is relatively open. The sympatric congener Celastrus scandens

108

is very similar to C. orbiculatus in both reproductive
biology and morphology. However, C. scandens is inferior to
C. orbiculatus in all reproductive characters observed in
this study. Celastrus orbiculatus produces more seeds that
are smaller and have a greater chance of germinating than
seeds of C. scandens. The smaller seed size and larger seed
number indicate that C. orbiculatus is more r—selected than
C. scandens. Following this argument, one would expect the
species with larger seeds to have a greater germination
success. But this study and others (Dreyer, Baird, and
Fickler 1987) have demonstrated lower germination success in
C. scandens. These findings imply that C. scandens is a poor
competitor relative to C. orbiculatus, and that the spread of
C. orbiculatus will continue. Further, it is possible that
the historically large distribution of C. scandens in
Michigan (52 counties) is currently dwindling and lacks
recruitment through seedling establishment. At the same time,
C. orbiculatus populations may be spreading through long
range dispersal of highly successful seeds. This spread may
be enhanced in disturbed sites, but the successful
germination of seeds under low light conditions in the
laboratory suggests that closed canopy sites may be invaded
as well.

Both C. orbiculatus and V1 riparia demonstrated similar

patterns of shoot elongation growth. Interestingly, both

109

species had greater shoot elongation under low light
conditions in the field, apparently as a “searching”
strategy. Additionally, both species were very similar in
phenology. These similarities were surprising, and suggest
that growth strategy overrides differences related to
taxonomy. The native liana V1 riparia does not appear to be
superior to C. orbiculatus in terms of shoot growth. Both
species demonstrated similar shoot elongation through two
growing seasons.

The invasion dynamics of C. orbiculatus do not appear to
be related to hydraulic advantages over native lianas.
Celastrus orbiculatus lacks the root pressure mechanism seen
in V3 riparia and lacks any advantage in hydraulic
conductance. These findings indicate that root pressure is
not a requisite characteristic for success as a temperate
liana. Cblastrus orbiculatus manages to thrive by producing
new xylem each year, even though this leads to a greater
commitment of resources to hydraulic tissues and hence wider
stems than V: riparia. It is important to note that the
larger annual incremental growth does not translate into
greater elongation of individual shoots. This fact is
demonstrated by the equivalent maximum shoot lengths seen in
C. orbiculatus and V1 riparia.

Dendrochronology is a useful and novel tool for the

reconstruction of liana invasion. No prior reports of

110

dendrochronology utilizing lianas are known, but this study
suggests temperate lianas should be considered as potential
sources of useful dendrochronological information. Liana
chronologies suggest establishment dates for C. orbiculatus
at each site, followed by successive recruitment. The
reconstruction of liana invasion events indicates that C.
orbiculatus continues to spread northward in Michigan. A
thorough sampling of C. orbiculatus populations throughout
Michigan would further establish the invasion dynamics
involved.

This study raises two important unanswered questions:
what limits sexual reproduction in C. scandens?, and what, if
anything, will limit the spread of C. orbiculatus? To
identify the limitations of reproduction in C. scandens, it
would be desirable to establish whether this species suffers
from inbreeding depression. The populations investigated in
this study produced copious amounts of seed that was
apparently viable as indicated by tetrazolium staining.
However, the seeds largely failed to germinate. Population
genetic information would be required to establish the
relatedness of individuals.

What could limit the spread of C. orbiculatus?
Minimizing the frequent and large scale disturbances
characteristic of many temperate ecosystems may help reduce

the opportunities for exotic species such as C. orbiculatus

111

to establish, persist, and invade. Massive eradication
efforts utilizing both removal and herbicide treatment can be
effective, though costly and risky to the native flora. There
may be opportunity for biological control by importing
natural enemies, insects or pathogens, from Asia.
Realistically, however, the current perception of threat by
C. orbiculatus invasion is too small to warrant such a
reaction. I believe that C. orbiculatus is here to stay. At

least it has attractive fruits!

112

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113

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