Butterfly Bush), on Plant Succession on New Zealand Floodplains

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Impacts of an invasive shrub, Buddleja davidii (butterfly bush), on plant succession on New Zealand floodplains

Nita Gay Tallent-Halsell University of Nevada, Las Vegas

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Repository Citation Tallent-Halsell, Nita Gay, "Impacts of an invasive shrub, Buddleja davidii (butterfly bush), on plant succession on New Zealand floodplains" (2008). UNLV Retrospective Theses & Dissertations. 2804. http://dx.doi.org/10.25669/r7df-d6qp

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This Dissertation has been accepted for inclusion in UNLV Retrospective Theses & Dissertations by an authorized administrator of Digital Scholarship@UNLV. For more information, please contact [email protected]. IMPACTS OF AN INVASIVE SHRUB, BUDDLEJA DAVIDIl

(BUTTERFLY BUSH), ON PLANT SUCCESSION

ON NEW ZEALAND

FLOODPLAINS

Nita Gay Tallent-Halsell

Bachelor of Science University of Nevada, Las Vegas 1989

Masters of Arts in Science University of Nevada, Las Vegas 1998

A thesis submitted in partial fulfillment of the requirements for the

Doctor of Philosophy Degree in Biological Sciences School of Life Sciences College of Sciences

Graduate College University of Nevada, Las Vegas May 2008

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Dissertation Approval The Graduate College University of Nevada, Las Vegas

April 2 08 - , 20_

The Dissertation prepared by

Nita Gay Tallent-Halsell

Entitled

Impact of an Invasive Shrub, Buddleja davidii (butterfly bush), on Plant Succession on New Zealand Floodplains

is approved in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Biological Sciences

Examination Committee Chair ?

Dean of the Graduate College

Examination Committee Member A A'A/-2^ Examination Committee Member Examination Committee Member ^ •

—A — ------Graduate C ollie Faculty Representative

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ABSTRACT

The Impact of an Invasive Shrub, Buddleja davidii (butterfly bush) on Plant Succession on New Zealand Floodplains

Nita Gay Tallent-Halsell

Dr. Lawrence R. Walker Committee Chair Professor of Plant Ecology University of Nevada, Las Vegas

Plant successional trajectories are driven in part hy the interactions among the biotic

and abiotic components of a plant community such that introduction of an invasive

species may impact the recruitment of native species. Buddleja davidii Franchet (Family

Buddlejaceae) is an ornamental shrub, native to China, able to rapidly colonize and

dominate disturbed areas around the world. This study details the impact B. davidii has

on several New Zealand floodplain communities and the recruitment, growth and survival

of a native species, Griselinia littoralis, in natural settings and under controlled

conditions in plots and treatments representative of a multi-stage (i.e., open, young,

vigorous and mature) developmental chronosequence (i.e., time since disturbance by

flooding). Although B. davidii was abundant on the floodplains studied from the open to

vigorous stages, it was rarely present as a mature plant. Soil phosphorus and nitrogen

concentrations increased along a developmental gradient which suggested that B. davidii iii

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. augmented soil nutrients over time. Growth of G. littoralis transplants under a B. davidii

canopy remained unchanged from the time they were initially planted in the open and

young stages yet nearly doubled in height in the vigorous stage suggests that B. davidii

may enhance the growth of G. littoralis transplants. The growth of the G. littoralis

transplants under the B. davidii canopy may have been facilitated by increased soil

moisture and nutrients. G. littoralis seedlings established naturally beneath the B. davidii

canopy, yet did not establish in the open or young stages. It appeared that B. davidii did

not inhibit G. littoralis establishment. B. davidii was not able to survive under the

relative darkness of a simulated vigorous developmental stage. Growth of G. littoralis

cuttings was suppressed by B. davidii in the open and young developmental stages yet G.

littoralis mortality was not negatively impacted by B. davidii. Although B. davidii

initially dominated the floodplain plant community, its influence may be temporary

because it cannot tolerate the closed canopy community of the later stages of succession

on New Zealand floodplains. Native species, able to tolerate a broader range of

conditions dominated the later stages of succession.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. TABLE OF CONTENTS

ABSTRACT...... iii

LIST OF TABLES...... vii

LIST OF FIGURES ...... viii

ACKNOWLEDGEMENTS...... x

CHAPTER 1 mTRODUCTION ...... 1 Plant Succession ...... 1 Biological Invasions ...... 4 Buddleja davidii ...... 8 New Zealand...... 10 Griselinia littoralis ...... 12 Floodplains ...... 14 The Impact of Invasive Species on Plant Successional Dynamics ...... 17

CHAPTER 2 THE INVASIVE BUDDLEJA DA VIDII (BUTTERFLY BUSH) 21 Abstract...... 21 Introduction ...... 22 Literature Review ...... 24 Conclusion ...... 60

CHAPTER 3 SUCCESSION ON NEW ZEALAND FLOODPLAINS DOMINATED BY AN INVASIVE SHRUB, BUDDLEJA DAVIDII...... 70 Abstract...... 70 Introduction ...... 71 Methods and Statistical Analysis ...... 76 Results...... 84 Discussion ...... 93

CHAPTER 4 THE INFLUENCE OF AN INVASIVE SHRUB, BUDDEJA DA VIDII ON A NATIVE SHRUB, GRISELINIA LITTORALIS TRANSPLANTED INTO A NEW ZEALAND FLOODPLAIN CHONOSEQUENCE...... 122 Abstract...... 122 Introduction ...... 123 Methods and Statistical Analysis ...... 126 Results...... 129 Discussion ...... 131

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 5 PLANT COMPETITION DURING SUCCESSION BETWEEN AN INVASIVE, BUDDLEJA DAVIDII AND A NATIVE, GRISELINIA LITTORALIS 149 Abstract ...... 149 Introduction ...... 150 Methods and Statistical Analysis ...... 151 Results...... 157 Discussion ...... 161

CHAPTER 6 CONCLUSION...... 181 Recommendations for Further Study ...... 185 Conclusion ...... 191

APPENDICES ...... On CD Appendix I Buddleja davidiiSurwey Catchment and River Characteristics Appendix II Buddleja davidnSmwey Species List and Characteristics Appendix III Buddleja riavir/h'-Survey Study Species List by Catchment Appendix IV Buddleja davidiiSmvQy Study Species List by Developmental Stage Appendix V Griselinia littoralis Transplant Experiment: Methods, Analysis and Results to Determine the Plant Community, Buddleja davidii Foliar Nutrients and Soil Properties and Chemistry for the Buddleja davidii-AommaiQà Plots Appendix VI Shade House Experiment; Least Square Means and Standard Error and f-values for Nutrient by Stage by Plant Treatment

REFERENCES...... 193

VITA...... 218

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. LIST OF TABLES

Table 3-1 Descriptive information about Buddleja riav/ri/i-Survey Catchments and R ivers...... 100 Table 3-2 Buddleja davidiiSmvQy Tests of Discriminant Dimensions ...... 101 Table 3-3 Buddleja davidii-E>m\Qy Standardized Discriminant Coefficients 101 Table 4-1 Griselinia littoralis-Transplant Experiment Tests of Discriminant Dimensions ...... 138 Table 4-2 Griselinia 7ittora/A-Transplant Experiment Standardized Discriminant coefficients ...... 138 Table 4-3 Results (ANOVA) for Griselinia littoralis Transplant Experiment 139 Table 5-1 Buddleja davidii and Griselina littoralis Plant Treatment Response Variables for Shade House Experiment ...... 166 Table 5-2 Buddleja davidii and Griselina littoralis Stage by Plant Treatment Response Variables for Shade House Experiment ...... 166 Table 5-3 General Linear Model Analysis for Shade house Experiment ...... 167

VII

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. LIST OF FIGURES

Figure 1 Illustration of Buddleja davidii Franchet...... 64 Figure 2 Provinces in China where Buddleja davidii occurs naturally ...... 65 Figure 3 Distribution of Buddleja davidii in the United Kingdom ...... 66 Figure 4 Distribution of naturalized Buddleja davidii in North A m erica ...... 67 Figure 5 Buddleja davidii seedlings in floodplain gravel soil ...... 68 Figure 6 Buddleja davidii on Conway River floodplain, South Island, New Zealand ...... 69 Figure 7 Stylized drawing of plant community development during succession 102 Figure 8 Examples of native New Zealand floodplain flora ...... 103 Figure 9 Locations of seven catchments where Buddleja davidii-Aommaied stands were surveyed on the South Island, New Zealand ...... 104 Figure 10 Examples of the four-stage developmental chronosequence from Buddleja davidii-dominaXQd floodplains ...... 105 Figure 11 Schematic of Buddleja davidii survey design ...... 106 Figure 12 Canonical dimensions for grouping Buddleja davidii developmental stages...... 107 Figure 13 Relationship between Buddleja davidii biomass and Buddleja davidii age.... 108 Figure 14 Plot of first and second factors with corresponding catchments identified 109 Figure 15 The plant species richness of 3 x 3 m Buddleja davidii-smvcy plots 110 Figure 16 Percentage of non-indigenous species of 3 x 3 m Buddleja davidii-sarvQy plots ...... I l l Figure 17 Percentage of woody plant species of 3 x 3 m Buddleja davidii-smvey plots 112 Figure 18 Buddleja davidii foliar N (%) and P (%) concentrations of 3 x 3 m Buddleja davidii-smwQy plots ...... 113 Figure 19 Soil bulk density of 3 x 3 m Buddleja davidii-?,mvQy plots ...... 114 Figure 20 Soil field capacity of 3 x 3 m Buddleja davidii-smvQy plots...... 115 Figure 21 Soil nitrogen (g m'^) of 3 x 3 m Buddleja Buddleja davidii-mrvQy plots .116 Figure 22 Relationship between soil nitrogen and Buddleja davidii biomass ...... 117 Figure 23 Soil organic carbon (g m'^) of 3 x 3 m Buddleja davidii-swycy plots 118 Figure 24 Relationship between soil organic carbon and Buddleja davidii biomass 119 Figure 25 Soil available phosphorus (g m'^) of 3 x 3 m Buddleja davidii -survey plots ...... 120 Figure 26 Relationship between soil available phosphorus and Buddleja davidii biomass ...... 121 Figure 27 Geographic locations of Griselinia littoralis transplant experiment floodplains...... 140 Figure 28 Schematic of Griselinia littoralis transplant experiment field layout 141

viii

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Figure 29 Griselinia littoralis transplants after 76 weeks ...... 142 Figure 30 Canonical dimensions for grouping Buddleja davidii r/evelopmental stages {Griselinia littoralis transplant experiment) ...... 143 Figure 31 Griselinia littoralis transplant shoot biomass ...... 144 Figure 32 Griselinia littoralis transplant growth ...... 145 Figure 33 Griselinia littoralis transplant specific leaf area ...... 146 Figure 34 Griselinia littoralis transplant root biomass ...... 147 Figure 35 Griselinia littoralis transplant root to shoot ratio ...... 148 Figure 36 Layout and description of shade house experiment ...... 168 Figure 37 Developmental stages and their shade house analogs ...... 169 Figure 38 Collection and experiment locations for Buddleja davidii and Griselinia littoralis shade house experiment ...... 170 Figure 39 Buddleja davidii and Griselinia littoralis cutting mortality after ca. 251 days ...... 171 Figure 40 Means and standard errors of Buddleja davidii and Griselinia littoralis cuttings plotted by stage and treatment ...... 172 Figure 41 Shoot relative growth rate of Buddleja davidii and Griselinia littoralis cuttings ...... 173 Figure 42 Root relative growth rate oi Buddleja davidii and Griselinia littoralis cuttings ...... 174 Figure 43 Root to shoot ratio Buddleja davidii and Griselinia littoralis cuttings 175 Figure 44 Specific leaf area of Buddleja davidii and Griselinia littoralis cuttings... 176 Figure 45 Foliar N of Buddleja davidii and Griselinia littoralis cuttings ...... 177 Figure 46 Foliar P of Buddleja davidii and Griselinia littoralis cuttings ...... 178 Figure 47 Buddleja davidii and Griselinia littoralis after ca. 251 days ...... 179 Figure 48 Buddleja davidii cuttings after different nutrient treatment {ca. 251 days) ...... 180

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ACKNOWLEDGMENTS

This dissertation is dedicated to my parents, Evelyn and Robert Tallent, my children,

Carey, Jesseeea, Jeremiah and Adam and my husband. Dr. Jeffrey Halsell, whose love

and support have been with me over the years and across the miles.

I have been incredibly blessed to be surrounded by so many wonderful people who

have either paved my way or walked beside me. I am indebted to Dr. Lawrence (Lars)

Walker for being my advisor and mentor throughout my graduate career. I am privileged

and honored to have had the opportunity to learn from him. In addition to being my

teacher, he has spent many hours teaching me the art of scientific writing with his red pen

and guiding me to see the world through the eyes of a scientist rather than as a tourist.

I owe much gratitude to many at the University of Nevada, Las Vegas, which I have

been a part of since 1985, including the members of my committee. Dr. Stan Smith and

Dr. Brenda Buck, and past professors and colleagues, especially Dr. Chad Cross, who has

encouraged me from the first day we met. I am most appreciative of the efforts of Dr.

Elizabeth Powell for improvements made to manuscript. In addition, I am grateful for the

Office of International Programs and the Graduate & Professional Students Association

for their support. I am indebted to Lauren Kominski, Will Hayes, Brian Necessary and

Jake Schimmel for their assistance in the lab.

Much appreciation is due to Dr. George Malanson for being on my committee.

Thank you for your confidence and the opportunity.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. I am forever grateful for the support I have received from my family at the US

Environmental Protection Agency. Much thanks to Dan Heggem, Ricardo Lopez, Bruce

Jones, Bob Shonbrod, John Lyon, Ann Pitchford and John Baker for supporting my

academic pursuits over the years. I am extremely thankful for my wonderful friends,

David Bradford, Aruiie Neale and Maliha Nash for their encouragement, council,

expertise and humor. I could never have made it this far without their willingness to

listen to me talk about Buddleja for hours on end. I am also thankful for the others who

have helped in many ways, big and small, Brian Schumacher, Katrina Varner, Kim

Johnson, Paula Allen, Jay Christensen and Terry Slonecker.

I am extremely thankful for Landcare Research in Lincoln, New Zealand for

accepting me as one of their own. It is wonderful to have family in New Zealand. I

made many new but lasting colleagues and friends from this experience. Cheers to Dr.

Duane Peltzer for being a member of my committee, all the invaluable assistance he

provided to make this project a reality and for welcoming me into “my home away from

home”. Also, special thanks are extended to Rob Allen, Vicki Allison, James Barringer,

Peter Bellingham, Stella Beiliss, Karen Boot, Ian Dickie, Stephen Ferris, George

Knights, Anna Langstrom, Chris Morse, Stuart Oliver, David Parcell, Helen Parish, Gaye

Rattery, Graeme Rogers, Melissa Thayer-Briggs, Graeme Ure, David Wardle, Marilyn

Watson, David Whitehead and Susan Wiser. Thank you Hiroko, danke shon Marc

Thomas and muchas gracias Pablo Manzano. Stella Beiliss, Terry Young, Susan Wiser

and Marilyn Watson, I will always appreciate that you opened your homes to me.

I am most grateful to Dr. Bruce Clarkson and Dr. Chrissen Grimmell for allowing me

to participate in the 2005 Flora of Aotearoa Summer Course (University of Waikato). xi

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Much thanks to Bruce, Chris, Catherine Beard and my fellow students who were

extremely knowledgeable, hospitable and fun.

Words cannot express the love and gratitude I have for my parents, Evelyn and

Robert Tallent who have been with me every step of the way. I thank them for taking me

out into the world before I could walk or talk and for making my life an incredible

adventure. I am truly blessed! Only with the support of my sisters, Terry and Jenny, my

brother Bob and my dear friend Carmen has this been possible. I am fortunate to have

them in my life. Many thanks to my new siblings, Carol Arm and Jonathan.

To my children, Carey, Jesseeea, Jeremiah and Adam, words cannot express the love

I have for them. Much thanks for enriching my life. Through their questions I have

learned so much. May they always follow their dreams!

Finally, I am especially appreciative of my husband. Dr. Jeffrey Flalsell. I do not

know how I would have completed my education without his enduring love, support,

patience and sense of humor. Thank you for sharing the years and miles together.

Xll

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 1

INTRODUCTION

Plant Succession

Plant succession is the pattern of change in vegetation after a disturbance has

removed plants, animals and microbes from above- and below-ground communities

(Horn 1974, Glenn-Lewin et al. 1992, McCook 1994, Walker and del Moral 2003). The

many complexities of any given environment at any moment in time drive the

successional dynamics that depend on the interactions between organisms and the

environment. Despite the stochastic nature of succession, successional patterns are

somewhat repeatable and the similarities among ecosystems worldwide suggest that

much of the pattern of vegetation dynamics may result from a few underlying processes

(Tilman 1985).

Connell and Slatyer (1977) identified the biotie interactions that influence

successional development as facilitation, tolerance and inhibition. Facilitation is the

positive influence of one species on another species. This influence promotes species

compositional change to the next successional stage (Walker and Chapin 1987, Callaway

and Walker 1997). Tolerance is when one species is able to tolerate lower resource

availability in the presence of dominant species. The tolerant species may eventually out-

compete the dominant species (e.g., shade toleranee in late successional species; Connell

and Slatyer 1977, Strong 2004). Inhibition is the negative effect of one species on

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. another. An inhibiting species may either slow or arrest successional change by

preventing the establishment of the other species (e.g., pre-emption by fast growing

plants or allelopathy; Wootton 2002, Walker and del Moral 2003, Gomez-Aparicio and

Canham 2008).

Primary succession is the establishment of plant assemblages on a landscape denuded

by the catastrophic removal of most plants, animals and soil microbes (e.g., following a

volcanic eruption; Walker and del Moral 2003). In contrast, secondary succession occurs

on landscapes that suffered an initial disturbance, but on which there is a substantial

biological legacy (i.e., hurricanes; Walker et al. 2003). During the secondary succession,

the plant community reassembles following a seemingly stochastic series of continuous

biotic and abiotic events (Horn 1974). These events influence which species will

reproduce, dominate or be replaced based environmental feedbacks (Chapin et al. 1994,

Luken 1990). Which species initially colonizes the community depends on the available

propagule pool, which could either be seeds in the seed bank or vegetative fragments that

are capable of developing roots (i.e., roots and stems; Butaye et al. 2002, Karmo and

Sewa 2004). Soil properties and water and light availability also influence species

recruitment (Tilman 1985).

The successional status of a plant species may be categorized based on a suite of life

history characteristics that confer success during a particular stage of succession (Bazzaz

1979, Huston and Smith). For example, plant species that colonize the open floodplain in

early succession generally have high rates of respiration, photosynthetic and water use

efficiency while species that will eventually dominate in late succession floodplain forest

have low rates of respiration, photosynthetie and water use efficiency that are adaptations

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. to the conditions beneath a closed canopy (Bazzaz 1979). Native plant assemblages are

the result of long periods of intra- and inter-specifie feedbacks that either inhibit or

encourage the establishment of individuals (Diaz and Cabido 2001).

Theoretically, communities, although never static, do settle into states of equilibrium

(i.e., climax community, steady state models; Clements 1916, McCook 1994). The

processes that favor recruitment are continuously adjusting in response to feedback loops

between below- and above-ground factors. However, the temporal and spatial scales at

which the community responds may be difficult to grasp. What we observe may be only

a snapshot in time perhaps following a long period of growth or preceding another period

of change. What we perceive as a stable community or patch might be a mosaic of

smaller patches responding to an array of above- and below-ground processes that are

shaping the system (Pickett and White 1985). We need to broaden our view to interpret

the past, observe the present and predict the future states of the plant community and

ecosystem properties from our snapshots so that we can determine the successional

trajectory that the system may take. However, the present structure may not necessarily

be indicative of its future condition.

Researchers have long sought generalized patterns of succession (Clements 1916,

1928, Gleason 1926, Gutierrez and Fey 1980, Anderson 1986, McCook 1994). If we

understand the short- and long-term patterns and processes that drive succession, we may

be able to predict future landscapes and facilitate conservation and restoration efforts

(Walker et al. 2007, Walker and del Moral in press). Generalized patterns of the

transitions and trajeetories of succession have been deseribed for watersheds, ecosystems,

plant communities and geographic locations based upon climate, soils, precipitation.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. topography and disturbance regimes (Glenn-Lewin and van der Maarel 1992, van der

Putten et al. 2001, Meiners 2007, Walker and del Moral in press). Processes that drive

succession have been well documented (Berkowitz et al. 1995, Walker and Vitousek

1991, Walker and del Moral 2003); however, the impacts of biotic invasions on these

processes are less well known.

Biological Invasions

Biological invasions are recognized as one of the most important causes of ecosystem

degradation and biodiversity loss worldwide (Vitousek et al. 1996, Mack et al. 2000).

Because of this, there has been extensive research on the expansion of species beyond

their native range. These species may be referred to by many names including non-

indigenous, non-native, naturalized, exotic, alien, weed and pest; however, the ability of

the organism to inflict ecological, economic damage or both on a specific system is

generally the foremost characteristic of concern (Cronk and Fuller 1995, Mack 1997,

Richardson et al. 2000, Davis and Thompson 2001, Colautti and Maclssac 2004).

Richardson and others (2000) suggest that the term ‘transformer species’ (originally

proposed by Wells et al. 1986) is a better descriptor when referring to a subset of invasive

plants that significantly change the “character, condition, form or nature of a natural

area”. Transformer invasives, whieh are approximately 10% of the invasive species

worldwide (Williamson 1996), often have a profound negative effect on biodiversity that

generates reaction from both the scientific community and the public. However, the

descriptor of transformer speeies as eeosystem transformers is not widely used in the

biological invasion literature. Consequently, throughout this paper and unless otherwise

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. noted, the preferred terms for this dissertation are “non-indigenous” to describe a species

that is not native to an ecosystem or to an geographic region, “naturalized’ to describe

non-indigenous species that reproduce consistently and sustain populations over many

life cycles without direct intervention by humans and “invasive” to describe species that

change the character, condition, form or nature of a natural ecosystem over a substantial

area.

If an invasive plant dominates an ecosystem, it can alter various community and

ecosystem properties and processes (i.e., succession; Walker and Smith 1997). Many

studies demonstrate that an invasive species’ impact on a community is greater than the

invader’s relative dominance in the community (Vitousek 1986, Smith and Knapp 2003,

White et al. 2006, Stayer et al. 2007, Peltzer et al. unpublished data). Invasives can alter

hydrology (Sala et al. 1996), fire regimes (Brooks et al. 2004), light penetration (Reinhart

et al. 2005), nitrogen cycling (Vitousek and Walker 1989) and myeorrhizal associations

(Stinson et al. 2007) and create allelopathie effects (Gomez-Aparicio and Canham 2008).

In addition, the economic consequences of invasions and cost of control can be

substantial (Mack et al. 2000, Pimentai et al. 2000, Cook et al. 2007). Research into the

impacts of invasive species on communities has contributed to our understanding of

biological interactions among species and how individual species can alter community

structure and ecosystems processes (Vitousek 1986, Lodge 1993, Walker and Smith

1997, Bruno et al. 2005).

The actual invasion of a community by a non-indigenous species is influenced by a

number of factors: the number of propagules entering the community (i.e., propagule

pressure; Lockwood et al. 2005), the characteristics of the non-indigenous species

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. (Daehler 2003) and the invasibility of the community (Williamson and Fitter 1996,

Lonsdale 1999). In addition, disturbance (i.e., any major event that disrupts ecosystem,

community or population structure and changes resources or substrate availability or the

physical environment; Pickett and White 1985, Walker 1999) is considered a major factor

in promoting plant invasions (Radosevich et al. 2003). Disturbance may be caused by

large-scale events such as fire, storms and floods, or smaller-scale events such as soil

turnover or vegetative removal by animals or humans (Walker et al. 2007). Native plant

communities generally respond somewhat predictably to periodic disturbance. There are

many theories proposed to explain why some communities are more invasible than

others.

Davis and others (2000) suggest that a plant community is more susceptible to

invasion when there is an increase in unused resources. Simply, a new speeies must have

access to available resources (e.g. light nutrients and water) to successfully move into and

reproduce in the community. An increase in resource availability is possible if there is a

decline in exploitation by native vegetation or because the rate of resource resupply is

faster than uptake by native vegetation (Davis and Pelsor 2001).

Conversely, many invasive plants have high resource use efficiency and persistence

in low-resource systems (Feng et al. 2007). Funk and Vitousek (2007) found that

invasive species can outperform natives over short and long timescales and may persist in

a community under conditions of continuous low-resource availability. Consequently,

invasive plants readily invade and dominate newly disturbed sites (Funk and Vitousek

2007). Non-indigenous organisms may become invasive outside their native habitat for a

number of reasons including release from native specialized herbivores (Mitchell and

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Power 2003) and higher relative growth rate in a habitat (Ebeling et al. 2008). Between-

species interaetions of the native species in the community, such as competitive

dominance, facilitation, mutualisms and herbivory can be altered by invasive species.

The fact that an invasive may usurp the ecological position of one or more of the

native species is of primary importance. Therefore, one of the main research questions

concerning succession after a non-indigenous plant invasion is to what extent the

successional trajectory may be altered in cases where resources (i.e., substrate and soil

nutrients) are no longer available. Altered successional trajectories can change

biodiversity and eeosystem productivity and stability, as well as have other consequences

on a community.

Many invasive plants have been introduced by the horticultural or agricultural

industries (Ewel et al. 1999, Reichard and White 2001, Williams and Cameron 2006,

Dehnen-Schmutz et al. 2007). Several past introductions have become “charismatie

weeds” that are valued by society; therefore, the threats they impose on ecosystems are

often not aeknowledged. Acer platanoides (Norway maple) was planted along suburban

avenues to replace Ulmus spp. (elms) that were decimated by Ophiostoma spp. infections

(i.e., Dutch elm disease) in the early 1900’s. Currently, Acer platanoides is highly prized

for its rich, green canopy and glorious fall foliage (Webb 2001). However, A.

platanoides has escaped from gardens and along roadways and established in natural

areas. As a result, Acer species native to North America have been replaced by A.

platanoides (Webb and Kaunzinger 1993).

Another example is Eichhornia crassipes (water hyacinth), which is appreciated by

many because it is an attractive water plant with dark green shiny leaves and beautiful

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. lilac-blue flower spikes. Despite the fact that it has been recognized as an invasive water

plant for more than 100 years, there is resistance to removing it from public ponds and it

can still be easily purchased from nurseries (Schmitz et al. 1993). The public’s

appreciation for these charismatic invasive plants, despite their ability to usurp and alter

native landscapes adds another level of complexity to the management of invasive

species (Leland 2005, Kaufman and Kaufman 2007).

Buddleja davidii

Buddleja davidii Franchet (family Buddlejaceae, common name butterfly bush),

native to China, is a large, multi-stemmed, semi-deciduous shrub that is cultivated as an

ornamental garden plant in temperate regions of the world. It is valued by landscapers,

gardeners, butterfly enthusiasts and bird watchers because it is easy to cultivate in

gardens and has flowers that attracts butterflies and birds. Buddleja davidii is welcomed

and celebrated by the general public because it is colorful and fragrant. Since B. davidii s

initial introduction to the United Kingdom in the late 1800s, the species has spread

widely across the Commonwealth, Europe and the United States. The species is a

concern for land managers because it establishes in disturbed areas, particularly riparian

habitats, floodplains, forest, clear cuts, road edges and railroad embankments (Chapter 2).

Buddleja davidii has many attributes characteristic of invasive plants (e.g., rapid

growth rate, high seed output, phenotypic plasticity; Baker 1965, 1974). The species is

drought- and flood-tolerant, rapidly colonizes disturbed areas and has a tolerance of a

wide spectrum of climatic conditions including oceanic, continental and Mediterranean

climates and (Chapter 2). Buddleja davidii readily establishes in a wide range of soil

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. types, including in coarse-textured, nitrogen-deficient soils (Humphries et al. 1982,

Humphries and Guarino 1987). The species increases soil nitrogen (N) and phosphorus

(P) in soils in which it is growing. The addition of phosphorus to soils by this species is

unique in contrast to native, N-fixing shrubs that do not also increase soil phosphorus

(Bellingham et al. 2005). Once B. davidii establishes it reproduces early and prolifically:

each shrub is capable of producing millions of wind-dispersed seeds (Miller 1984,

Wilson et al. 2004, Thomas 2007). Buddleja davidii has an extensive, fast growing root

system that produces adventitious shoots and roots on fragments of buried or cut stems.

The species is semi-deciduous (i.e., the species can immediately replace leaves dropped

in autumn and spring). This feature allows B. davidii to optimize the length of the

growing season. Buddleja davidii accumulates phosphorus via rapid root proliferation

and myeorrhizal associations (Dickie et al. 2007). Furthermore, B. davidii can establish

as dense thickets that may affect river hydrology and geomorphology (Leach 2007).

In New Zealand, B. davidii is a relatively short-lived (i.e., < 30 yrs) perennial. The

species appears to colonize in high densities in the first 10 years of life (Smale 1990).

Bellingham and others (2005) report that 70-80% of a New Zealand floodplain plant

community in early successional stages was dominated by B. davidii, but dominance

declined to about 15% by the mature stage. Buddleja davidii was able to dominate early

floodplain succession by establishing in high densities after flooding exposed substrate

suitable for recruitment sooner than native pioneer species (Bellingham et al. 2005).

However, mamre vegetative stands in the same floodplain were dominated by native

species (Bellingham et al. 2005). This suggests that B. davidifs dominance may be

relatively short-lived. The long-term impact of B. davidii dominating early plant

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. succession on biotic interactions among native plant species is unknown. Several

researchers have suggested that B. davidii is capable of facilitating and altering

successional trajectories and thereby negatively affecting biodiversity and ecosystem

productivity (Williams 1979, Miller 1984, Gibb 1994, Brown 1990, Smale 1990,

Richardson et al. 1996, Williams and Wiser 2004, Bellingham et al. 2005).

New Zealand

New Zealand is a country in the south-western Pacific Ocean comprising two large

islands (the North Island and the South Island) and numerous smaller islands with a total

land area of ca. 270,000 km^. Most notable for its geographic isolation, New Zealand

nearest neighbor, Australia, is more than 1,600 km to the northwest (Hutching 1998).

New Zealand’s mild and temperate climate is influenced by the surrounding ocean,

tropical wind patterns, its location in a latitude zone (ranging from approximately 34 to

47°S) with prevailing westerly winds and mountain chains that extend the length of New

Zealand (McKnight 1994).

New Zealand is located on the boundary of the Pacific and Indo-Australian tectonic

plates that has shaped its landforms. Earthquakes and volcanic and geothermal activity

have produced mountainous terrain over more than two-thirds of the combined islands

land mass (McKnight 1994). The landscape has been impacted by volcanic emptions,

some of which were catastrophic in recorded history (i.e., Mt. Taupo eruption ca. 181

AD) and localized lightning-sparked fires.

The post-glacial period in New Zealand was characterized by a gradual warming that

culminated about 8000 years ago. Since that time, the climatic regimes have oscillated

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. around an average similar to, but slightly warmer and wetter than today (Newsome

1987). These comparatively minor fluctuations in climate probably had an unsettling

effect upon the vegetation, which resulted in frequent shifts in plant distribution.

However, the longevity of many forest trees and even larger tussock grasses would have

served to smooth out the more extreme climatic fluctuations (Wardle 1991).

Because of New Zealand’s long isolation from other land masses (i.e., ca. 80 million

yr since separation from Gondwanaland) and its island biogeography, 80% of New

Zealand’s flora is endemic, including 65 endemic genera (Hutching 1998). The New

Zealand flora has evolved adaptations to most natural disturbances, but has evolved in the

absence of predation by mammals. A special feature of the ecological range of New

Zealand forest plants is the virtual absence of “intolerant” species (Dansereau 1964).

Intolerant species are equally able to germinate and establish in the open as in dense

shade. The patterns of successional stages that typically develop after disturbance on

floodplains in temperate regions (i.e., open to herbaceous dicots to woody shrubs to trees)

are evident in New Zealand systems; however, the native species prevalent within one

stage are not necessarily replaced in another stage; rather the dominance among species

may shift overtime (Dansereau 1964, Wilson 1990).

The introduction of humans and mammalian herbivores in recent history has changed

the character of disturbance of native plant communities from slight to extensive and

fundamentally catastrophic (Newsome 1987). Initially settled by the Eastern Polynesians

who came to New Zealand, probably in a series of migrations, sometime between 800

and 1300 AD, New Zealand was later colonized by Europeans beginning in the late

1700s (Smith 2005). After the colonization of the islands by humans, the landscape

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. rapidly changed from a primarily forested landscape to lowlands dominated by open

habitat with fragments of native vegetation (Mooney and Hobbs 2000). The herbaceous

plants of the riverbed communities, prior to the mass immigration of Europeans to New

Zealand, would have been dominated by perennial dicot and monocot herbs (e.g.,

Epilobium spp., Raoulia spp., Cortaderia spp.), small-scrubs (e.g., Coprosma spp.,

Carmichaelia spp.) and short woody plants (e.g., Discaria toumatou\ Cockayne 1927,

Cockayne and Foweraker 1916, Foweraker 1916, Wardle 1991, Williams and Wiser

2004). Ruderal species (annuals) were very rare (Dansereau 1964).

Currently, only a vestige of the native vegetation remains on floodplains in New

Zealand (Cumberland 1941, Wardle 1991, Allen and Lee 2006). The prevalence of

Eurasian species in New Zealand’s register of exotic plants reflects the persistent efforts

of 19* century colonists to the New Zealand islands to create a “Better Britain” in the

Southern Hemisphere. The flora of New Zealand also represents a number of Eurasian

stowaways (Lusk and Bellingham 2004). In the past 200 years, many New Zealand

floodplains have been intensively managed for agriculture and horticulture and have

become dominated by invasive non-indigneous grasses, herbs, shrubs and trees (e.g.,

Bromus spp. Taraxacum officinale, B. davidii and Salix fragilis, respectively; Brown

1990, Smale 1990, Timmons and Williams 1991,Wardle 1991, Gibb 1994, Williams and

Wiser 2004, Bellingham et al. 2005, Williams and Cameron 2006).

Griselinia littoralis

Griselinia littoralis Raoul Choix (family Griseliniaceae; Allen 1982, Reveal 2008) is

a dioecious tree endemic to New Zealand that can be epiphytic (i.e., grows upon or

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. attached to another living plant; Wardle 1991). The species has a widespread distribution

from lowland to subalpine habitats from 35° 30’ latitude southward including the North,

South and Steward Islands. Griselinia littoralis is an early to late successional species;

however, the successional status of New Zealand plants are often difficult to classify

because many New Zealand plants can germinate, establish and reproduce across a range

of light and moisture regimes (Dansereau 1964). A mature G. littoralis tree has

spreading branches and a gnarled main stem and can grow to a height of 15 m in deeply

shaded to well-lit environments (Burrows 1995). Sometimes G. littoralis dominates

patches in forests that have been altered by fires, landslides or other disturbances. In

addition, G. littoralis is found as an understory or canopy species in mixed angiosperm-

podocarp o t Nothofagus forests (Wardle 1991). Griselinia littoralis has been distributed

around the world. The species is used in landscaping, and has naturalized in the United

Kingdom and Europe (Clement and Foster 1994, Preston et al. 2002, Hill et al. 2005,

Wallentinus 2008).

Griselinia littoralis has short-stalked, berry-like fruits that are consumed by birds that

distribute the seeds in their feces (Burrows 1995). Each fruit has a single seed that has

thin, soft seed coat surrounded by a thin, but not juicy pericarp. Baylis (1959, 1961,

1967) considered G. littoralis a relatively slow growing species. Griselinia littoralis has

a vesieular-arbuseular mycorrhizal association that facilitates phosphorus (?) uptake

(Baylis 1959, 1961, 1967); however, uptake is regulated by plant need rather than P

availability in the soil. Griselinia littoralis is strongly mycotrophic and therefore

responds only weakly to added P. This suggests that the speeies has evolved a growth

rate compatible with the low concentrations of available P in New Zealand soils (Baylis

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 1967, White and Lovell 1984). Also, slow-growing and shade-tolerant species such as G.

littoralis generally have a lower percentage of mycorrhizal roots in comparison with

other comparable native fast-growing light-responsive speeies (Baylis 1967).

Floodplains

Floodplains are land areas adjacent to a river, stream or waterway that are subject to

recurring inundation (Leopold et al. 1964). The floodplains along the braided gravel-bed

rivers in New Zealand are generally extensive landforms composed of gravel bars and

islands. These islands are usually physically unstable and have high turnover (Gray and

Harding 2007). Despite this, biologieal communities survive in the floodplain beeause

the relative proportion of each kind of habitat (i.e., open, channel islands, elevated

riparian forest) in any particular floodplain remains roughly constant over time (i.e., in a

state of dynamic stability; Latterell et al. 2006, Gray and Harding 2007). The shifting-

mosaic steady states of floodplains make them ideal for conducting research on plant

succession (Whited et al. 2007).

Three mechanisms contribute to floodplain dynamies: 1) High magnitude flow

events, which cause river bed abandonment due to lateral migration of the channel and

localized river or channel incision (Reinsfelds and Nanson 1993) 2) surface water that

flows over the alluvial gravel bed and 3) ground water that move vertically and

horizontally through the gravel beds (Woessner 2000).

Two physical gradients influence the floodplain; the longitudinal gradient, which is

characteristic of the regional location of the river and distinguished by local (i.e., the

length of the river from headwater to mouth; Malanson 1993) and the transverse gradient

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. that depends upon the width, geology and geomorphology of the local charmel (i.e.,

perpendicular to the channel). The longitudinal gradient of the floodplain can represent a

continuum of plant species distributed from the mountainous headwaters to the lowlands

and can span across a range of erosional to depositional zones within the floodplain, that

have areas of dynamic equilibrium or transportional zones between.

On the South Island of New Zealand, alpine rivers are characterized by large floods

that result from heavy rain and snow melt along the main divide (Harding and Gray

2007). Floods are common in spring and early summer. In contrast, the flows are low in

winter because water is retained in the upper catchment in the form of snow and ice. In

late summer and autumn flow are low because precipitation levels are low.

On a floodplain there are gradients of plant establishment on new substrates based on

biotic interactions among plants, the physiological tolerance of plants to flood duration

and frequency as well as water table depths (Malanson 1993). This means that although a

particular plant community may be destroyed in one place, it will remain intact or be

forming in others (Harding and Gray 2007). Furthermore, the existence of plant

communities in different successional stages provides a highly diverse mosaic of

floodplain communities, each with its own spatially and temporally distinct character and

structure (Hauer and Lorang 2004). The stability of the communities is much higher

when islands and bars have mature vegetation (Malanson 1993). However, periodic high

power floods can completely rework the channel removing all biota above- and below-

ground (Harding and Gray 2007).

A recent study that investigated the influence of flooding on river morphology on the

lower Waimakariri River (South Island, New Zealand) revealed that the river turns over

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. two-thirds of its available floodplain annually (>0.2 m vertical erosion or deposition) and

would probably re-work the entire floodplain in 5 years (Hicks et al. 2008). This

demonstrates the dramatic influence that water movement can have on a floodplain plant

community. The floodplain bed is made up of water-worn gravels from the size of fine

sand to boulders. The range in particle size affords many microenvironments that can

impact colonization of plants (Walker et al. 2006). Seasonal winds can dry and

destabilize the surface particles further shaping the substrate and influencing plant

colonization.

The floodplain vegetative community reflects a legacy of hydrologie conditions, from

large scouring floods that create expansive barren areas open for recruitment, to extended

periods of moderate to low disturbance that promote succession. River flows of low to

moderate power that are relatively frequent and predictable scour portions of the

floodplain, and create areas that are free of vegetation and therefore, available for early

successional processes to occur (Fisher et al. 1998). These flood events may result in the

stimulation of seed germination and therefore vegetative expansion of riparian vegetation

depending upon the availability of suitable microsites on the floodplain after the flood

(i.e., microsites are small scale sites with the larger floodplain that are fertile and provide

stability and protection from drought and predation; Walker et al. 2006).

Soil properties and chemistry, the availability of soil moisture and plant tolerance to

drought and flooding shape the plant community (Hughes 1997). Plants on the

floodplains are found along a gradient corresponding to time since last disturbance.

Terraces and within channel islands that are higher in elevation than the river bed (and

therefore less often flooded) generally have the oldest plant communities and low lying

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. areas that are frequently flooded may be intermittently populated by seedlings. However,

the vegetation establish along gradients of other factors such as moisture, nutrient or light

availability which may or may not be correlated with time or flood frequency Because of

the dynamic hydrology and the physiological requirements of the vegetation, the

floodplain is generally a shifting mosaic of various species of plants of different ages that

reflect the microsite conditions at the time of recruitment and the complex array of

stressors that follow through time (Hughes 1997).

The Impact of Invasive Species on Plant Successional Dynamics

An important step toward management and control of invasive species is

understanding the factors that affect the abundance and distribution of an invading

species. There is no coherent body of scientific information on the factors promoting B.

davidii invasions or long-term effects of B. davidii on native plant communities. We do

loiow that B. davidii has colonized on floodplains throughout New Zealand for no less

than 60 years; however, the impacts of long-term establishment across the landscape are

unknown (Williams 1979, Smale 1990, Gibb 1994, Bellingham et al. 2005). Therefore, it

has been difficult to generalize about the effects of B. davidii establishment on native

ecosystems.

New Zealand floodplains are ideal locations to study the impact of B. davidii on

succession. Naturally reoccurring disturbances on these floodplains drive the cyclic

vegetation dynamics that within the past two hundred years have been altered by the

introduction of B. davidii. Therefore, we can use the introduction of B. davidii in New

Zealand to understand whether short-term dominance of an invasive species can produce

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. long-term impacts on a plant community that has evolved to tolerate reoccurring

disturbance.

Although the best way to determine how an invasive species may impact a native

system is to study a species on a particular area for a long time, this approach may be

logistically infeasible and slow to return timely answers. A short-term approach to

reconstructing long-term dynamics are chronosequences (Strayer et al 2006). Using a

chronosequence that represent different stages of succession infers a time sequence of

plant development from a series of plots differing in age (Johnson and Miyanishi 2008).

The assumption is that each stand in the sequence differs only in age and that each stand

has the same history in both its abiotic and biotic components (Johnson and Miyanishi

2008). The chronosequence method has been a surrogate for repeated measurements of

community succession for decades (Pickett 1988, Sturtevant et al. 1997, Fraver et al.

2002).

Bellingham and colleagues used a four-stage developmental chronosequence of time

since last flood to study the impact of B. davidii on the Kowhai River, South Island, New

Zealand (Bellingham et al. 2005). They defined the stages as; 1) “open” (mostly

unvegetated; seedlings <0.5 fn tall), 2) “young” (plant canopy had not coalesced; plants

0.5-2 m tall), 3) “vigorous” (complete plant canopy cover; plants 2-4 m tall), and 4)

“mature” (closed plant canopy; some senescing individuals; plants > 4 m tall; Bellingham

et al., 2005). The assumption was that each developmental stage of the floodplain plant

community would have repeated the successional sequence of every other older stage up

to its present age. Changes in plant species composition, nutrient sequestration and soil

fertility were detected among the developmental stages that were dominated by B.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. davidii. However, whether these patterns were unique to this river or repeated in other

rivers are unknown.

Investigating plant community and ecosystem properties on a four-stage

developmental chronosequence of time since last disturbance by floods on other New

Zealand floodplains can provide information about the long-term impact of B. davidii.

The assumption being that a developmental chronosequence of plant communities

dominated by B. davidii is a suitable surrogate for the different stages of plant succession

in plant communities dominated by B. davidii. The three overall objectives addressed by

this dissertation are:

1) to investigate the impact that an invasive species, B. davidii, has on New Zealand

floodplain plant communities dominated by B. davidii and ecosystem processes in a

four-stage developmental chronosequence

2) to test how 5. davidii will influence a native species, G. littoralis, in B. davidii-

dominated floodplain plant communities in different stages of development

3) to test the interaction between B. davidii and G. littoralis in a controlled setting

that simulates different stages of plant community development.

In order to address these objectives I conducted three separate research projects that

are described in the following chapters. This chapter has provided a review of the current

literature on plant succession and plant invasions with an emphasis on floodplains in New

Zealand. Chapter 2 provides a review of the literature about the history, distribution,

ecology and management of B. davidii. Chapter 3 addresses the hypothesis that the

impact of 5. davidii on plant community composition, soil properties and chemistry will

vary over time and along an environmental gradient. I used vegetation surveys and soil

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. analysis of a four-stage developmental chronosequence (i.e., time since disturbance by

last flood) on seven New Zealand floodplains to examine the variation in the pattern of

succession of plant communities on those floodplains. In Chapter 4 ,1 hypothesize that B.

davidii will impact the growth of G. littoralis transplanted in a chronosequence oîB .

r/ov/r/i/'-dominated stands. However, the positive (e.g., facilitative) and negative (e.g.,

competitive inhibition) impacts will vary based on the developmental stage of the plant

community.

The experiment described in Chapter 5 examines the hypothesis that B. davidii has an

impact on G. littoralis but that the impact is contingent on the successional stage. The

experiment was conducted in controlled shade houses where light and nutrient levels

were applied in a full factorial design. The review of the literature and the observations

made during these experiments offer an opportunity to examine the effects of an invasive

species {B. davidii) on plant successional dynamics on a New Zealand floodplain.

Chapter 6 is a summary of Chapters 1 through 5 and provides recommendations for

future study.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 2

THE INVASIVE BUDDLEJA DAVIDII (BUTTERFLY BUSH)

Abstract .

Buddleja davidii Franchet (Synonym. Buddleia davidii', common name Butterfly

bush) is a perennial, semi-deciduous shrub or small multi-stemmed tree that is resident in

gardens and disturbed areas in temperate locations worldwide. Since its introduction to

the United Kingdom from central and western China in the late 1800s, the tree has

become an important component in horticulture and human culture. Despite its

popularity as a landscape plant, B. davidii is considered problematic because of its ability

to naturalize outside of gardens and rapidly invade and dominate disturbed natural areas.

There is concern that the species has negative and irreversible impacts on the agricultural

and wild lands it has invaded. Around the world, B. davidii is an opportunist that is able

to tolerate a wide range of physical conditions. Buddleja davidii is highly prolific. A

single tree is capable of producing millions of wind- and water-dispersed seeds and can

propagate vegetatively by way of stem and root fragments. The species has a rapid

growth rate, high specific leaf area and high foliar nitrogen and phosphorus levels relative

to other native woody shrub species. These attributes increase the plant’s photosynthetic

efficiency and competitive capabilities. Buddleja davidii has an arbuscular mychorrhizal

association and therefore, is an efficient phosphorus accumulator. The species displays a

high degree of phenotypic plasticity and consequently has been able to expand beyond

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. the environmental limits of the plant’s native habitat. The species has a low

susceptibility to disease and herbivory. Although B. davidii is a successful colonist,

whether the species can alter successional trajectories over the long term has not yet been

determined. The ecological, horticultural and economic impacts of B. davidii must be

determined in order for best management practices to be implemented. The primary goal

of this paper is to synthesize what is known about B. davidii so that ecologists,

horticulturalists, land managers and others can understand the impacts caused by the

continued presence of B. davidii in gardens and natural landscapes. I also address

management of B. davidii and discuss the repercussions of various management

strategies and policies currently implemented to protect or remove B. davidii from natural

ecosystems.

Introduction

Buddleja davidii Franchet is a perennial, semi-deciduous shrub or small multi

stemmed tree that readily establishes on disturbed areas in temperate locations. Native to

central and western China, B. davidii has been introduced as an ornamental to the

Americas, New Zealand, Australia and Europe because of it fragrant and eolorful flowers

(Synonym. Buddleia davidii, Buddlea davidii', Buddleia variabilis Hemsl., Buddleia

magnijica Hort, Buddleia nanoensis Hort; Bailey and Bailey 1976, Bricknell and

Zukl997; Family Buddlejaceae; Common names: butterfly bush, orange-eyed butterfly

bush, summer lilac).

In the 100 years since B. davidii’’s introduction, the tree has spread from gardens to

disturbed and natural areas including floodplains, railroad and road edges, forest bums

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. and clear-cuts. Horticulturalists, landscapers, gardeners, butterfly enthusiasts, bird

watchers and the general public welcome and celebrate B. davidii’s colorful and fragrant

place in urbanized landscapes (Coats 1992, Dirr 1997, Dole 1997, Klingaman 2002,

Savonen 2004, Wilson et al. 2004a, Forrest 2006, Stuart 2006, KCGG 2008). However,

many others consider B. davidii invasive and problematic. There is concern that it has

potential negative and irreversible impacts on agricultural and wild lands it invades

(Richardson et al. 1996, Reichard and Hamilton 1997, Anisko and Im 2001, Reinhardt et

al. 2003, Wilson et al. 2004b, PIER 2005, WSNWCB 2006).

The desire to protect the continued presence of B. davidii in gardens is matched by

the concern by land managers to control B. davidii. It is clear that B. davidii is an

important component of both horticulture and society (Stuart 2006). Considering the

level of interest in B. davidii by both the public and land managers, a thorough

understanding of the ecological impacts of B. davidii naturalization over the long-term is

required.

Despite research on the distribution, ecology, physiology, and management of B.

davidii gaps exist in our knowledge about native and non-indigenous B. davidii. The

primary goal of this paper is to synthesize what is known about B. davidii so that

ecologists, horticulturalists and others can fully appreciate the impacts of the continued

presence of B. davidii in gardens and natural landscapes, and understand the

repercussions of management efforts. This review of the literature eonceming B. davidii

is divided into six sections; history, taxonomy, distribution, biology, ecology and

management.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Literature review

History of Buddleia davidii

Buddleja davidii was introduced to Europe in 1869 by French missionary, Father

David from the Moupine Province, East Tibet, and, again, by Dr. Augustine Henry

(Nelson 1980) in 1887 from the I-ch’ang Province of China. The genus Buddleja was

named in honor of the English amateur botanist. Rev. Adam Buddie (Chittenden et al.

1951). The species was named after Father David who collected and returned specimens

of the Chinese flora and fauna to Adrien René Franchet at the Paris Musée National

d’Historie Naturelle (Bean 1970). David sent Franchet specimens of B. davidii in 1869

(Franchet 1884, 1888). Specimens of the same species from I-ch’ang Province were

collected by Henry and named by the William Botting Hemsley in 1887 (Anon. 1925).

Unaware of Franchet’s description, Hemsley called the plant B. variabilis Hemsl

(Hemsley 1889). The name was eventually reversed 25 years later, due to the discovery

of Franchet’s original description. However, B. variabilis is still listed as a synonym of

B. davidii.

Buddleja davidii seeds were first introduced to Europe from Russia by traders (Bean

1970). These seeds were reported to produce, from a horticulture perspective, an inferior

form (Bean 1970, Coats 1992). A second form was introduced to Louis DeVilmorin of

France from Tatsienlu, China, in 1893 by Jean André Soulié (Herberman 1919). This

form produced what was considered a superior plant (i.e., erect habit, flowers in denser

and longer panicles; Cox 1986). Once grown, the plant resembled B. davidii var.

veitchiana that was later introduced to Britain by Ernest Wilson (National Council for the

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Conservation of Plants and Gardens 2007). DeVilmorin sent seed from the Tatsienlu

specimens to the Kew Gardens in 1896 (Coats 1992).

Further collections of seeds were sent from Mt. O’mei Shan, China in 1896 by

another French missionary (and botanist) Father Paul Guillaume Farges

(ThePlantExplorers.com 2007) and in the following year by Henry from I-ch’ang.

Wilson collected B. davidii for its numerous and attractive seed capsules (not flowers) in

the Hupeh and Szechwan regions of China during the years 1907-1910 from which the

common garden-variety B. davidii descended (Rehder 1927, Bean 1970). However,

some of the naturalized plants in Britain may have originated from the earlier seed

collections or from hybrids with the original stocks Miller (1984).

There is an on-going debate surrounding the spelling of the genus B. davidii. Dr.

William Houstoun, a British naval surgeon and botanist who retrieved plants from

Mexico and South America (Steams 1988), originally proposed naming specimens he

collected in the West Indies {ca 1730-33) Buddlea to commemorate Rev. Buddie (Miller

1835). Houstoun’s B. davidii specimens were named by Linnaeus B. americana in his

Species Plantarum (1753) and Genera Plantarum (1754). Hemsley (1989) and Robinson

(1898), introduced the species to English gardeners in different weekly horticultural

journals as Buddleia. Bean (1970) spelled the genus Buddleia as well. Other versions,

such as Budlaea, Budlea, and Buddleya have all been published (Coats 1992).

Miller (1984) suggested that Houstoun may have used the tailed “i” in his spelling of

Buddleja (the 1 looks like a j), which was prevalent in the 1700s when an author wished

to denote a consonant sound. However, Gillman (in Pellet 2007) argued that...

“Linnaeus did not spell Buddleja correctly” and speculated that typesetters of the time

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. used “j”s for “i”s, as well as using “v”s for “u”s and “P’s for “s”s in the main text, yet not

in the indexes. In Linnaeus’ work on plant systematics (1789) Buddleja with a “j” was

written in the text, yet was listed in the index with an “i” thus suggesting that Linnaeus

intended that it should have been spelled Buddleia with an “i”. Nevertheless, according

to the International Rules of Nomenclature, Article 24 states that genera names can be

taken from any source whatever and may even be composed in an absolutely arbitrary

manner. Therefore, the spelling adopted by Linnaeus in 1753 and 1754 must be retained

(Sprague 1928) regardless of whether the name resulted from errors or misinterpretations.

I follow Sprague’s recommendation and spell Buddleja with a “j ”.

Taxonomv of Buddleia davidii

The Family Buddlejaceae

The classification of the genus Buddleja has been in flux for some time. Originally

ascribed to the family Scrophulariaceae by De Jussieu (1789) and Lindley (1846), it was

later reclassified in the Loganiaceae by Bentham (1857). Later,Wilhelm (1910) gave

Buddlejaceae family rank next to the Loganiaceae (Norman 2000). Leeuwenberg (1979)

treated Buddleja and its allies as a tribe of Loganiaceae.

Embryological studies indicate that Buddlejaceae is close to the Scrophulariaceae.

Yet, Scrophulariaceae does not have stipules as does the genus Buddleja. Houghton and

others (2003) excluded the genus Buddleja from the Loganiaceae based on

chemosystematic aspects of terpenoids (iridoid and aucubin) present in the plants and

suggested that the genus should be included in a new taxon including the

Scrophulariaceae and Lamiaceae. However, the convention at present is to place the

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. genus Buddleja and other related genera in the family Buddlejaceae based on seed and

embryonic characters (Oxelman et al. 1999, Olmstead et al. 2001).

The Buddlejaceae consists of angiosperms that are trees, shrubs or lianas that are self-

supporting or climbing. A majority of the genera in Buddlejaceae are found in the Old

World, except for Emoiya (Norman 2000). The eight genera in Buddlejaceae occur in

warm, tropical climates (Norman 2000); Androya (one species, Madagascar); Buddleja,

(ca. 100 species and cultivars, native to the Americas, Africa and Asia); Emorya (one

species, Texas and Mexico); Gomphostigma (two species. South Africa); Nuxia (fifteen

species, southern Arabia and tropical Africa); Peltanthera (one species, tropical

America); Polypremum (one species, warm regions in America); and Sanango (one

species, Ecuador). The African genera Adenoplusia and Nicodemia were recently

reclassified in Buddleja (Adkins 2004). There are no native plants of the Buddlejaceae in

Australia, New Zealand, or Europe (Stuart 2006).

Chromosomal analyses indicate that the basic chromosome numbers of this family are

7 and 19 (Moore 1947, Norman, 2000). Ploidy levels recorded are 2, 4, 6, 12, 16 and 38.

About 48% of species in the genus Buddleja have been described based on differences in

cytology. Both New and Old World polyploids have been identified (Adkins 2004).

Polyploidy appears most frequently in Asian species (Moore 1947, 1960). Chen and

others (2006, 2007) found the basic chromosome number of 27 populations of 14

Buddleja species, was x = 19 with the presence of several ploidy levels . Specifically, the

species B. davidii has a tetraploid number of 2n = 76 (Chen et al. 2007).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. The Genus Buddleja

The genus Buddleja is a cosmopolitan genus of Buddlejaceae consisting of

approximately 100 species in the tropical and temperate zones of the world (Marquand

1930, Norman 2000, Chin et al. 2007). Four Buddleja species have particularly wide

distributions: B. americana (Central America south into northwestern regions of South

America), B. salvifolia (Africa; Angola and Kenya south to South Africa), B. asiatica

(from Eastern India into China) and B. crispa (Afghanistan east to Kansu Province in

China; Stuart 2006). However, many species o ïBuddleja are localized and often found

in isolated valleys or mountainsides (e.g., B. utahensis grows only in the Washington

region of southwestern Utah).

The pan-tropical distribution of the genus Buddleja and the limited extent of the

other genera in Buddlejaceae suggests that the genus Buddleja originated in South Africa

and that the other genera in the family evolved from Buddleja (Norman 2000). New

World diversity in the family is centered in southeastern Brazil, the Andes, Central

America, and the southwestern United States. These regions account for approximately

63% of the species in the genus (Norman 2000). The diversity of Old World Buddleja

species is centered in Africa (ca. 15%) and the Sino-Himalayan region of South-east

Asia (ca. 21% Leeuwenberg 1979, Li and Leeuwenberg 1996, Norman 2000). Although

higher diversity of Buddleja species exists in Asia and the Americas, some researchers

accept the proposal put forth by Moore (1960) that Africa is the generic origin of

Buddleja species world wide (Oxelman et al. 1999, Norman 2000, Adkins and Wemer

2003, Adkins 2004).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. The advanced features of Buddleja species floral morphology and the fact that the

flowers are adapted for pollination by species in the evolutionarily advanced insect orders

of Hymenoptera and Lepidoptera suggests that the genus may have arisen in the early

Tertiary period at a time when seasonal variations in day length drove the climatic

segregation of floras (Moore 1961). Photoperiodism and the polyploidy of the genus give

further evidence that the genus is advanced (Moore 1961). Advanced species are often

positively correlated with complex cytology (i.e., polyploidy). Moore (1961) correlated

flowering habit (required length of day for flowering) of the genus Buddleja with

evolutionary level and polyploidy. He concluded that, in general, all diploid (except B.

lindleyana) and one polyploid Buddleja species were short-day plants, and thus more

primitive in evolutionary origin, in contrast, all other polyploid Buddleja species are

long-day plants, which he considered more advanced in origin.

Buddleja davidii Franchet

Seven subspecies of B. davidii and 90 B. davidii cultivars have been described

(Stuart 2006). The subspecies from various locations in China, were originally

introduced at different times to the United Kingdom (Marquand 1930) and generally vary

in overall plant size, length of the inflorescence, size and color of flower, and the color of

the leaves. Some of these varieties are now considered heirloom plants that gain and fall

in popularity over time (Findley et al. 2004, Stuart 2006).

Buddleja davidii breeding programs began as early as 1920, when W. van de Weyer

developed interspecific hybrids resulting from crosses between B. globosa and B.

magnifica (Wilson et al. 2004a). Since that time, cultivars have been bred for size, a

variety of flower colors and environmental hardiness for the nursery trade. Several

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. hybridization programs were initiated in the late 1990s under the direction of M. A. Dirr,

J. T. Lindstrom, and D. J. Wemer (Dirr 2001, Gaus and Adkins 2002, Lindstorm et al.

2002, Adkins and Wemer 2003, Rendfro and Lindstorm 2003, Lindstorm et al. 2004).

These plant hydridization programs have focused on flower color, inflorescence

morphology, compact growth habit, gray pubescent foliage. The development of sterile

plants, and novel B. davidii hybrids have been created with the use of less common

species. The cross between B. davidii and B. fallowiana is named B. davidii ‘Lochinch’

(Wigtownshire, Scotland). B. davidii ‘Lochinch’ was thought to be sterile and therefore

an ideal alternative to the B. davidii. However, field observations reveal that the hybrid

reproduces abundantly by seeds and shows invasive characteristics (EPPO 2005).

In addition to developing cultivars to exploit size (dwarfness; Podaras 2005) and

hardiness, and to enhance flower and leaf eolor (Lindstrom et al. 2004, Podaras 2005),

eultivars are sought to reduce inherent invasibility (CANR 1998, 2007). J. Ruter,

University of Georgia, (CANR 2007) is experimenting with gamma irradiation

techniques to induce sterility in B. davidii cultivars. J. Lindstrom, University of Arkansas

and P. Podaras, Cornell University, are working independently on B. davidii hybrids that

are sterile (Podaras 2005). Lindstorm and others (2002, 2004) have sought to reduce

potential invasiveness by producing hybrids that either alter plant morphology

(speeifically seed or fruit characteristics) or have an odd ploidy number. These

researchers have used genetic engineering techniques to produce hybrids with dwarfed or

nonfunctional reproductive organs or that produce heavier seeds that are not carried by

the wind.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Podaras (2005) has generated B. davidii crosses with distantly related Buddleja

cousins to produce pollen-sterile plants. In addition to being sterile, these hybrid plants

are more shade-tolerant than their parents. Offspring also exhibit flowers that are more

than twice the size of their female progenitor, (B. davidii ‘White Profusion’). It has been

confirmed that Buddleja polyploids have been crossed to diploids to create sterile triploid

mules (Podaras 2005).

Buddleja davidii are shrubs or small multi-stemmed trees that have a great degree of

morphological and physiological plasticity (Miller 1984, Shi et al. 2006). Buddleja

davidii may be found as solitary individuals or in dense thickets. Some individuals have

a spreading habit, able to repeatedly grow from the base of the plant creating a total basal

area of 40 - 50 cm. The entire plant may extend over an area of 2-3 m^. Other

individuals may have a single, slender, stem with a total cover of less than 1 m '\

Descriptions of B. davidii may vary slightly depending on the environment. In

general, stems are four-angled. Suborbicular to ovate stipules are present and range in

size from 1 -6 mm. The leaves are usually ovate (less commonly lanceolate) and shortly

petiolate. The upper surfaces of the leaves are dark green and glabrous or free of hairs;

below they are whitish to greyish tomentose (covered with many fine hairs) with stellate

and glanduliferous hairs (Webb et al. 1988, Leeuwenberg 1979, Zheng and Raven 1996).

Leaf edges are serrated. Leaves are wedge shaped, narrowing to a point. Leaves range in

size from 5-20 cm long and 1-7 cm wide (Zheng and Raven 1996). The glanduliferous

hairs borne on the leaves and stems extrude crystals giving a characteristic sheen that

enable identification of seedlings. See Figure 1 for an illustration of some taxonomic

features of B. davidii.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Buddleja davidii is semi-deciduous: leaves are shed in the autumn and immediately

replaced with a set of new, smaller leaves that persist until the following spring. The

autumn leaves are covered with downy hairs. During the spring B. davidii produces a

flush of leaves . Both spring shoots and leaves are pubescent, however the hairs

disappear as the year progresses (Miller 1984).

Buddleja davidii can tolerate severe eold (-28.8°C; Stuart 2006); however, cold

hardiness varies among cultivars. Most cold hardy cultivars have an origin that is closest

to the original form from northwestern China (Podaras 2005). In colder climates,

cultivars bred for milder climates, will shed all leaves and stems and produces new shoots

in the spring (Coats 1992). Without winter die-back, several cultivars would grow too

large for some gardens (Podaras 2005). Considered a USDA zone 5 plant (Podaras

2005), the roots of most B. davidii cultivar need to be protected in colder extremes of its

cultivated range.

Buddleja davidii is unique because the main meristem grows underground and is not

carried aerially as it is in many woody species. As a result, the plant has no main trunk.

Instead, several stems originate from the belowground meristem. In favorable seasons,

the apical meristem of each of the stems will continue to grow in successive springs with

few lateral branehes and new growth is concentrated behind the old seed heads (Miller

1984). In the winter, the aerial shoots die or may be broken and new shoots arise from

underground in the spring. Gardeners have long recommended eutting back old wood in

the autumn for optimal shoot growth and flowering the next year (Savonen 2003,

Turnbull 2004). However, the ability to survive winter is enhanced when plants are not

cut back (Warr et al. 2002). The underground meristem enables clonal growth that

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. explains the extensive thickets of even-aged plants that establish in disturbed areas

(Miller 1984). The lack of an apical meristem makes determing the age of B. davidii

difficult. However, some authors have suggested (based mostly on succession) that

naturalized non-indigenous plants may live to be greater than >30 yrs or about 20 yrs

(Kowhai River, South Island and central North Island, New Zealand, respectively; Smale,

1990; Bellingham et al., 2005).

Distribution

Native Distribution

Buddelja davidii is native to temperate central and southwestern China at elevations

up to 3500 m (Fig. 2). The native range of B. davidii are the Chinese provinces; Gansu,

Guangdong, Gaungxi, Guizhou, Hubei, Hunan, Jiangsu, Jiangxi, Shaanxi, Sichuan,

Xizang, Yunnan and Zhejiang where it can be found as thickets on mountainous slopes

(Starr et al. 2003, Stuart 2006). Wilson (1913) describes stands of B. davidii in

bottomlands and abandoned cultivated areas in the northwestern Szechuan Province as

“...thousands of bushes, each one with masses of violet-purple flowers, delighting the

eye on all sides.” Comprehensive range maps of B. davidii are not available for the

native or introduced ranges (Ebeling et al. 2008).

Introduced Range

The Industrial Revolution in Europe led to the rise of the middle class, which led to

an increase in the number of personal gardens enclosed in and around European towns

(Miller 1984). In particular, the practice of including exotic species in gardens became

popular during the Victorian Age (Thacker 1979). No emphasis was placed on

preventing the spread of these introduced species. Only a few species introdueed from

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. the Far East at that time were able to survive outside of gardens and arboreta. One of

these species was B. davidii.

Several species of Buddleja including B. davidii were introduced to Europe in the

late 1800s and became popular additions to English gardens by the end of the IQ'** century

(Robinson 1898, Webb 1985). Prior to 1935, there were few incidents of B. davidii

reported naturalized outside of gardens UK (Miller 1984). It is probable that B. davidii

had escaped earlier than 1935 from gardens because the species seeded freely in gardens

and therefore, had the potential for dispersal and establishment outside of the garden

(Thurston 1930). The Institute of Terrestrial Ecology, Biological Records Centre records

suggested that B. davidii first became naturalized on a significant scale in the 1930s in

limestone quarries, on old walls, and on areas of exposed chalk in Great Britian (Fig. 3a;

Owen and Whiteway 1980).

Naturalized B. davidii populations expanded, especially in urban areas, after the

destruction of European cities during World War II. Bombed sites and building rubble

were suitable colonization habitat, and therefore dense B. davidii thickets established on

these sites (Miller 1984, Coats 1992). In the 1950s and 60s in the United Kingdom, B.

davidii became a popular garden shrub, which further contributed to its escape from

cultivation and naturalization in the wild (Owen and Whiteway, 1980, Miller 1984).

Local floras provided a description of B. davidii distribution post 1945 (Miller 1984);

Buddleja davidii appeared to have spread originally along rail tracks. The rock and

gravel that lined the railroad were ideal B. davidii habitat and seeds were carried long

distances on trains and along the railroad corridor (Miller 1980). Dereliction of railway

lines continues to enable B. davidii encroachment (Blacker 2007).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Buddleja davidii is currently well established in United Kingdom, primarily in

disturbed areas (Anisko and Im 2001, Stokes et al. 2004, Doughty 2007). A comparison

of distribution in 1984 and 2008 (National Biodiversity Network 2007) indicates that B.

davidii in the United Kingdom has increased by 83% (Fig. 3a-b). Buddleja davidii is one

of the most common and widely distributed naturalized non-indigenous plant species in

the United Kingdom flora (Webb 1985, Thompson et al. 2005):“It is ... likely that

Buddleia [i'/c] occurs as a garden plant or as an escape in almost every town in the British

Isles” (Owen and Whiteway 1980). The National Biodiversity Vascular Plant Database

(Botanical Society of British Isles 2007) lists over 6 000 incidences of B. davidii in

United Kingdom (Fig. 3b).

Buddleja davidii distribution in Europe has been noted as extending from the

Mediterranean to Bergen, Norway (Sheppard et al. 2006). The distribution is probably

restricted between oceanic and suboceanic climates in the temperate and

submediterranean zones (Ebeling et al. 2008). The eastern range margin currently

extends throughout Germany (Ebeling et al. 2008). Further spread North may be

restricted by the species’ lack of frost tolerance (Kunick 1970). In France, B. davidii is

present in the Paris basin, Pyrenees mountain, Gironde Esturay, Provance of Brittany and

Department of Alpes-Maritimes (ISSG 2007). Buddleja davidii was the most frequently

encountered species in wastelands in Brussels, Belgium (Godefroid et al. 2007).

Interestingly, B. davidii is a component of plant communities that grow specifically on

old stone walls and in the cracks of walls in Europe (Rishbeth 1949, Segal 1969).

Buddleja davidii is distributed throughout Africa (Lebrun and Stork 1992-1997,

Germisuizen and Meyer, 2003, Dobignard, in prep.) and was introduced to several Asian

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. countries, such as Japan and South Korea, where the species is not native, (Stuart 2006).

Soon after being introduced to Europe (ca. 1900), B. davidii was brought to North

America. The species probably escaped cultivation along the eastern coastline and now

occurs from Pennsylvania to North Carolina. On the west coast, the speeies oecurs from

California to Canada (Fig. 4; Reichard 1996, NatureServe 2007).

The spread of B. davidii is probably directly related to the spread of British citizens

to British colonies around the world. These colonists brought with them familiar garden

plants (Lusk and Bellingham 2004, Williams and Cameron 2006). Colonists spread B.

davidii to all the world’s continents and islands, including New Zealand. The only

continent in the world that apparently has not yet been invaded by this plant is Antarctica.

The first reference to B. davidii (Buddlea [^/c]) in the New Zealand literature was in a

1930 publication about butterflies in New Zealand (Patterson 1930). It was not until

1946 that the species was recorded naturalized outside of gardens (Healy 1946).

Currently, the species is naturalized in the North Island and common in the northern half

of the South Island of New Zealand, but less common in the southern half of the South

Island (Esler 1988, Webb et al. 1988, Gibb 1994)

Bioloev

Flowering, fruiting and seed production

Buddleja davidii cultivars occur in colors ranging from white to yellow and red, but it

is the common lilac and purple varieties that occur in the wild (Stuart 2006). Each B.

davidii flower is made up of four petals that are fused for three-quarters of their length

into a corolla tube. Individual plants, as well as flowers, show a wide range of

morphological plasticity: some plants bear mostly 4-petalled flowers, but also are

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. expressed as variants possessing 5-9 petals in one flower. These variants usually oecur in

the middle of the inflorescence (Fig. 1(1); Miller 1984). The flowers are zygomorphic,

possessing four stamens with filaments fused to the corolla wall and anthers situated

about two-thirds along the length of the tube. The corolla tub is 5-8 mm long, opening at

the top to form separate petals. Generally, this part of the flower is colored a variant of

purple, while the interior of the flower is orange with a series of yellow nectar guides

lead to the interior of the tube (Fig. 1(4)). This intense orange-yellow spot at the base of

the inner surface of the corolla tube of each Buddleja flower can be attributed to a

diterpene (non-cyclic crocetin-gentiobiose ester). This diester is used as a yellow

colorant in foods (Aoki et al. 2001, Houghton et al. 2003). Fine hairs line the length of

the tube, and are most dense at the top. The superior ovary is bilocular with a stigma and

style that extend along one third of the tube, and ends well short of the anthers. There is

a small ring of sepals around the base of the corolla tube. The corolla tube elongates until

it is 3 to 4 times the length of the sepals, before the petals finally open. Flowers have

minute pedicels, if any (Leeuwenberg 1979).

Buddleja davidii inflorescences are indeterminant corymbose-panicles that can extend

up to 30 cm in length (Findley et al. 1997). Some inflorescences may be densely

massed, others may be sparsely assembled around the stem (Miller 1984). Each stem

normally bears one large terminal inflorescence and two smaller lateral panicles arising

directly behind it (Miller 1984). Flowering is asynchronous (Miller 1984). Each panicle

consists of individual flowers that mature acropetally from the base to the top of the

inflorescence (Findley et al. 1997). Buddleja davidii typically flowers for several weeks

in mid-summer to early autumn (northern hemisphere May to October; Zheng and Raven,

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 1996; southern hemisphere December to February, rarely until April; Webb et al. 1988),

yet can be variable in flowering time from year to year. Individual flowers last for 1 -3

days and a panicle may persist for > 2 weeks (Findley et al. 1997). Miller (1984) found

that the date of first flowering varied between individuals and in different locations in the

United Kingdom.

Fitter and Fitter (2002) reported that B. davidii’s first average flowering dates in the

1990’s in the United Kingdom were delayed by 36 days in comparison to average dates

from data collected between 1954 and 1990. Conversely, the majority of the 557 plant

species observed by Fitter and Fitter (2002) flowered earlier in the 1990s than the period

prior to 1990. Flowering time, which is sensitive to temperature, may have changed in

direct response to climate-warming. These changes have the potential to disrupt plant

community dynamics, alter competition regimes and other interactions (Fitter and Fitter

2002, Grossman 2004). Why the increase of temperature appears to delay flowering in

cultivated B. davidii and at the same time promote earlier flowering in a majority of other

plants should be investigated . Findley and others (1997) found that exposing B. davidii

cultivars to elevated, twice-ambient ozone concentrations delayed first flowering date by

4 days.

Seeds are produced within three weeks of first flowering. The seed capsules are

brown, narrowly ellipsoid to narrowly ovoid. 5 - 9 x 1.5 -2 mm, acute at the apex,

narrowed towards the base, mostly 3-4 times as long as the calyx, and are often smooth,

or have stellate hairs (Fig. 1(5); Zheng and Raven 1996; Wilson et al. 2004b). The

capsule has an impressed line along the line of dehiscence (Leeuwenberg 1979). The

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. flowers are borne upright, which apparently favors pollinating insects and enables ready

dissemination of seeds from the capsule (Miller 1984).

Seeds are medium brown, thread-like, and long-winged, and are borne in a cylindrical

two-valved capsule. The fine seeds range in size from 3-4 x 0.5 mm with the center

slightly thickened (Fig. 1(6); Norman 2000). The seed body is no more than 0.5 mm in

length and < 0.06 mg in weight (Comelissen et al. 1996). Seeds are also minutely

reticulate, with long wings (axial placentas) at each end. Seeds are arranged tightly

packed, with their long sides aligned with the axis of the capsule (Miller 1984).

Buddleja davidii does not self-pollinate and therefore depends on insect pollinators

(Miller 1984). The absence of self-pollination has been linked to the heavy allocation of

resources to insect attractants in other species and therefore, may explain the presence of

conspicuous flowers both in color and size, pungent scent and abundant nectar in B.

davidii (Miller 1984, Houghton et al. 2003). A single mature B. davidii individual can

produce millions of seeds; however, estimates of the number of seeds produced vary

(100,000 to 3,000,000) among 5. davidii cultivars (Miller 1984, Brown 1990, Wilson et

al. 2004b, Thomas 2007). Seed formation and ripening typically occurs within three

weeks after flowering (maturing in the autumn; Miller 1984, Stuart 2006).

Dispersal

Naturalized B. davidii plants in the United Kingdom retain seeds on the plant

throughout winter, and then release the seeds in early spring into summer (Miller 1984).

During arid periods, the sides of the seed capsules dry and curl outward (Miller 1984).

The distal ends of the capsule open outwardly, which exposes them to the air and enables

seeds to disperse if there is sufficient air movement to shake them free of the capsule

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. (Miller 1984, Stuart 2006). With an increase in humidity, the capsule closes (in less than

five minutes) and dispersal ceases until the humidity declines again. Buddleja davidii in

Oregon does not release its seeds until mid to late winter (Ream 2006). Buddleja davidii

in New Zealand has been observed to release seeds in late autumn through early winter

(D. Peltzer and M. Thomas, pers. comm., N. Tallent-Halsell pers. obs.).

Seed dispersal may take place over an extended period of time depending on the

conditions (Miller 1984, Wilson et al. 2004b). Seeds dispersed prematurely were

confirmed to be less viable than those retained in the capsule (Miller 1984). Once

released, the majority (95%) seeds of an individual B. davidii plant are dispersed 10 m or

greater beyond the parent (Miller 1984). Buddleja davidii seeds can remain airborne for

prolonged periods once they are caught by the wind (Miller 1984).

Buddleja davidii seeds are also reported to be water-dispersed, especially along sea

coasts, floodplains and riparian corridors (Miller 1984, Webb et al. 1988, Brown 1990).

Seeds can be washed downstream during flood events, where they can establish in new

habitats (ISSG 2005). In addition. Lippe and Kowarik (2006) found that automobiles and

other vehicles can disperse B. davidii seeds. Seeds have been observed in the mud stuck

to machinery (N. Tallent-Halsell pers. obs.).

Plants readily reproduce asexually from stem and root fragments (Miller 1984, Smale

1990). Buddleja davidii individuals that has been disturbed by flooding and mechanical

means has been observed regenerating from buried stems, stumps and roots soon after the

disruption (N. Tallent-Halsell pers. obs.). Buddleja davidii debris, left after removal

attempts, can regenerate, flower, and spread, if left in on site on floodplains (H. Turnbull

pers. comm.).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Soil Seed Bank

Buddleja davidii seeds, in situ, can remain dormant for many years (Thompson et al.

2005). Laboratory experiments revealed that seed viability in the laboratory remained

high up to 2 years (Miller 1984). Stuart (2006) advised seed eollectors that garden B.

davidii seeds stored in dark, dry and cool (frost free) conditions can remain viable for

years. Several environmental factors such as soil type and moisture, seed depth, seed

predation and microbial and fungal activity contribute to the removal of B. davidii from

the seed bank (Miller 1984). In a survey of gardens in the United Kingdom, Thompson

and others (2005) found B. davidii seeds were the most abundant non-indigenous seeds in

the various seed banks. Buddleja davidii seeds have also been found in woodland

seedbanks in the United Kingdom (Warr et al. 1994).

Germination

Within 24 hours after the B. davidii is seed hydrated, the seed releases a yellow

pigment (the composition and function of which is unknown; Miller 1984). The

membranous outer seed coat, which has two wings for dispersal, swells during imbibition

to form a sheath in which the embryo expands and the radicle elongates. The radicle

ruptures the seed coat at a point about half-way along the length of a wing (Miller 1984).

Immediately before the seed ruptures, a circular ring of fine hairs, originating from the

junction between the hypocotyl and the epicotyl extends through the seed coat. The hairs

apparently function as initial absorptive organs: the hairs absorb water that may support

the rapid expansion and proliferation of cells in the subsequent stages of development.

Once the radicle has emerged, the gap in the seed coat is widened by the growth of the

hypocotyl until the cotyledons are drawn out behind it. Although the seedling is

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. completely free of the seed coat at this stage, it can remain attached to the cotyledons for

several days (Miller 1984). Germinants produce roots that may extend more than 10 cm,

branch multiple times yet remain near the surface, within the first three weeks before

shoot development begins (i.e., before the extension of the cotyledons; Miller 1984).

Soil moisture content is critical for germination. Germination requires a period of

imbibition of at least 5 days (Miller 1984). In the field, an input of at least 20 cm of rain

over a short period was noted by Miller (1984) as required to produce seedlings.

Buddleja davidii germinated over a range of temperatures from 15 to 29°C (Miller 1984).

Seeds tested at 9°C did not become metabolically active. The metabolic rate is faster at

higher temperatures with the optimum temperature around 24 “C (Miller 1984). Exposure

to ambient light is important for germination (i.e.. Based on comparison between an

average photosynthetic photon flux of 84 pmof^ s'^ for 12-h photoperiod and complete

darkness; Wilson et al. 2004b), irrespective of temperature (i.e., the range tested was

between 10 and 25°C; Wilson et al. 2004b).

Buddleja davidii seeds do not demonstrate irmate dormancy (Miller 1984). The seeds

are highly sensitive to burial to depths greater than 1 cm. This is typical of taxa with no

period of seed dormancy. Buddleja davidii seeds were not found to be capable of

germinating under anaerobie conditions, or very low (1.05%) oxygen tension (Miller

1984). However, there was no significant difference in the final germination at or above

5% oxygen. Miller (1984) concluded that the level of oxygen did not limit the

colonization by B. davidii. The effect of soil pH (i.e., the range tested was between 4 and

11) on B. davidii seeds was determined to be negligible (Miller 1984). Intraspecific

allelopathy also had no direct effect on B. davidii germination.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Growth and metabolism

Seedling shoots are obtusely angled, floccose (appear cottony ) and tomentose

(having very fine hairs on the surface) when young (Zheng and Raven 1996).

Germinants up to four weeks old are sensitive to drought. After four weeks, seedlings

become drought-tolerant (Feng et al. 2007). Seedlings can grow on a N-poor substrate.

Also, seedlings require full sun (Feng et al. 2007). Initial seedling survival may be

enhanced by microsites of gravel and stone shelters found on floodplains (Miller 1984).

Stony soils are well aerated and provide numerous microsites in which atmospheric

humidity can increase, preventing desiccation of the seed and seedlings (Fig. 5).

However, there is no evidence that B. davidii dominates New Zealand floodplains by

establishing in different microsite types than native species (Walker et al. 2006).

Buddleja davidii is fast-growing and has been reported to be able to increase between

0.5 and 2m in height annually. Seedling stem diameter can increase annually by as mueh

as 1 cm yr ' (Owen and Whiteway 1980, Miller 1984, Dunwell and Cappiello 2000,

Thomas 2007, Ebeling et al. 2008). An average increase in height of 6.3 mm d ’ of

several cultivars grown from cuttings has been recorded (Dunwell and Cappiello 2000).

Buddleja davidii seeding mean relative growth rate (RGR mean ± SE 0.200 ± 0.0048 g d'

', n = 36) was among the fastest reported by Comelissen and others (1996) in a

comparison of the seedling growth of 80 woody species from the United Kingdom and

North Spain. A flush of B. davidii plants established on a building rubbish heap, grew to

an average height of 2 m and flowered in one season. Within the next three to four years,

the thicket formed with an average height of more than 4 m high (Owen and Whiteway

1980).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Saplings display a high degree of phenotypic variation depending on micro and

macrosite conditions. Under experimental conditions, decreased spacing of B. davidii

plants negatively influenced stem branching and height (Armitage and Dirr 1995).

Buddleja davidii growth and flowering declined when exposed to ozone both

experimentally and in the field compared to plants grown without ozone enhancement

(Findley et al. 1997).

Buddleja davidii roots grow rapidly and develop extensive networks of fine roots.

Main root development extends down 4 m or more in the soil (Miller 1984) and roots are

capable of surviving damage sustained during flooding and mechanical removal.

Buddleja davidii accumulates soil phosphorus (Bellingham et al. 2005, Dickie et al.

2007). Although Harley and Harley (1987) reported B. davidii as non-mychorrhizal,

Camargo-Ricalde and others (2003) found B. davidii spp. (species unidentified) in

Mexico as possessing arbuscular myehorrhizal (AM) fungal structures. Dickie and others

(2007) confirmed the presence of AM in B. davidii in New Zealand, the United Kingdom.

It is highly likely that North American B. davidii also have arbuscular mychorrize.

The life span of B. davidii is variable. Individual plants may not live for more than

20 years. Plants older than 20 years were found to die from stem rot (Smale 1990,

Binggeli 1999). However, B. davidii > 30 yrs old were found at the Kowhai River, South

Island, New Zealand (i.e.. Based on aerial photographs and B. davidii tree ring counts;

Bellingham et al. 2005). Not only are individual shrubs short lived, but so, too are

stands o f B. davidii. Smale (1990) found that seedling density is initially high during the

first year of establishment. He estimated that there were more than 1,000,000 of

seedlings within one hectare in the western Ikawhenua Range and in the upper Waioeka

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. catchment, Urewera National Park, North Island, New Zealand. After one year stem

density decreased to 13,000 ha ’ due to self-thinning. Mature stands of B. davidii had 2

500 shrubs per hectare after 10 years. At the Kowhai River, South Island, New Zealand,

Bellingham and others (2005) inferred self-thinning occurred during B. davidii stand

development.

Eeologv

Habitat

Around the world, native and non-indigenous B. davidii is an opportunist that readily

establishes in natural and disturbed areas and is able to tolerate a wide range of physical

conditions (Fig. 6; Wilson 1913, Williams 1979, Miller 1984, Smale 1990, Reinhardt et

al. 2003, Bellingham et al. 2005, Godefroid et al. 2007). In both its native and introduced

range, B. davidii establishes naturally or on anthropogenieally disturbed sites such as

quarries, urban waste grounds, abandoned cultivated areas, along transport corridors

(Godefroid et al. 2007), and on walls and rock faces (Wilson 1913, Rishbeth 1949, Segal

1969, Miller 1984, Owen and Whiteway 2000). Buddleja davidii’s ability to withstand

the extreme environment of the disturbed landscape may enable it to fill vacant niches

(Rohde 2005, Woodley 2006). /

Naturalized B. davidii have been found to establish outside the environmental limits

of B. davidii populations native to China probably because of the species’ broad

environmental tolerances and high degree of morphological and phenotypic plasticity

(Ebeling et al. 2008). Ebeling and others (2008) found that German populations of B.

davidii were significantly taller and had thicker stems, larger inflorescences and heavier

seeds than plants from the species’ native Chinese populations. These variations in

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. performance were not attributed to climatic differences between the two geographic areas

because, on average, the Chinese populations experienced higher temperatures and

precipitation as well as a longer growing season than did the German populations.

Natural enemies, herbivores and predators on B. davidii in China apparently reduce plant

growth and reproductive success oiB. davidii populations in China. The lack of these

predators may contribute to the invasion success of B. davidii in Central Europe (Ebeling

et al. 2008).

Buddleja davidii is able to establish on piles of calcium based building debris and

masonry walls (Owen and Whiteway 1980, Miller 1984, Goderfroid et al. 2007).

Surveys of B. davidii thickets in disturbed areas of southern England (Miller 1984) and

Belgium (Godefroid et al. 2007) found that soils on which these thickets established were

high in sand, nutrient poor, and high in calcareous substrates (including concrete and

building debris). Yet B. davidii does not appear to be an obligate calcicole: It is able to

flourish in ealcium-deficient soils as well (Humphries and Guarino 1987). Miller (1984)

and Goderfroid and others (2007) have found that B. davidii was capable of colonizing

areas with a high pH. Dolomitic lime additions increased B. davidii growth by increasing

the uptake of Ca++ and Mg++ availability (Gillman et al 1998). Furthermore, in soils

with high concentrations of ammonium B. davidii plants were less susceptible to

ammonium toxicity than a native plant, Betulapendula (Humphries and Guarino 1987).

The presence of B. davidii in coastal areas suggests that it is able to tolerate the low

moisture content of sand and gravel substrates, as well as the desiccating and damaging

effects of the salt-laden onshore winds.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. In a study of riverbed elevation, substrate ,and landform in the Tolt River,

Washington, USA, Leach (2007) found no consistent patterns of B. davidii seedling

establishment. However, higher densities of persistent B. davidii plants were present at

higher elevations on streambank terraces and sheltered locations compared to native

Populus spp.or Salix spp.. This suggests that B. davidii is less tolerant of high shear

stress and prolonged inundation than either native tree {Populus or Salix). In addition, B.

davidii crown shoots contributed more to overall channel roughness than either of the

native species. This indicates that colonization by B. davidii could accelerate rates of

local sediment accretion. Buddleja davidii also has a greater density of fine roots than

Populus. This indicates that eolonization by B. davidii may result in increased bank

strength. Accelerated rates of sediment accretion and an inerease in bank stability could

lead to the development of more persistent in-channel landforms, and decrease rates of

channel migration (Leach 2007).

Biotic Interactions

Buddleja davidii seedlings and saplings are able to grow in high densities within

small groups and are not subject to self-thinning until a much later stage of suceessional

development (Miller 1984, Smale 1990, Bellingham et al. 2005). Individuals were

capable of persisting in relatively dense stands under conditions of intraspecific

competition.

Buddleja davidii seems to have both an inhibitory and facilitative influence on co

occurring native plants. Field surveys and experiments have demonstrated that B. davidii

is shade-intolerant. The absence of B. davidii seedlings beneath dense B. davidii thickets

(Miller 1984, Bellingham et al. 2005) is apparently due to competition for light, not self-

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. allelopathy (Miller 1984). Shade-intolerance has apparently evolved in this species

because it is not specifically advantageous for seedlings to establish beneath their parents

where competition for water and other resources may be a major factor for survival.

Ttherefore, it appears to be advantageous for the seeds of this species to be dispersed

away from the parent. Only 5% of seeds of naturalized B. davidii plant studied in the

United Kingdom fell within 10 m of the parent plant while ca 95% were dispersed >10

m (Miller 1984). In Oregon, USA, B. davidii seed dispersal distance ranged between 3 -

15 m (Ream 2006). This dispersal strategy may be advantageous to early colonizing

species because it may reduce the likelihood of out-crossing between siblings and self

(Miller 1984).

Succession

Although B. davidii colonizes disturbed sites, whether it alters suceessional

trajectories over the long term is yet undetermined. To address the impact that B. davidii

may have on suceessional trajectories in disturbed habitats Miller (1984) surveyed the

dispersal pattern and densities of 5. davidii in three different stages of the plant’s life

cycle as it established in an abandoned gravel pit in Slindon, West Sussex, United

Kingdom. The three stages chosen by Miller represented the establishment patterns seen

throughout the United Kingdom, and ranged from isolated individuals to dense,

seemingly even-aged thickets (Miller 1984). Her analysis did not reveal a high level of

intraspecific competition nor predictable development sequences of vegetation associated

with the presence of B. davidii.

Segal (1969) found B. davidii to be a late colonizer in a survey of vegetation

established on European walls. Only when the wall is in a fairly advanced state of

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. decomposition does B. davidii establish in the “mural community” and thus B. davidii is a

late suceessional introduction, only able to survive under later conditions (Segal 1969).

Buddleja davidii is an example of a species in which size and reproductive output are

generally lower when the species grows on extreme habitats than when the individuals

grows in more suitable habitats (Segal 1969).

Williams (1979) and Smale (1990) speculated, based on his observations, that B.

davidii would alter the course of plant succession in Urewera National Park, North

Island, New Zealand. Buddleja davidii quickly displaced primary native colonizers, both

herbaceous, and woody species such as Kunzea encodes on New Zealand floodplains.

This accelerated the reforestation process in streambeds. However, flooding would reset

the reforestation often enough to prevent woody forest from permanently establishing

(Smale 1990). Buddleja davidii dominated the earliest stages of primary succession on

the Kowhai River floodplain. South Island, New Zealand and had several novel impacts

on soil nutrients and species diversity in a comparison with native colonizers (Bellingham

et al. 2005).

Morphological and Physiological Traits

Buddleja davidii when introduced in disturbed environments often becomes dominant

because the species has apparently evolved attributes such as high reproductive and

dispersal capabilities, rapid seedling establishment, wide phenotypic plasticity, greater

growth-related characteristics, low susceptibility to herbivory and disease and

competitive abilities as long as resource availability remains optimal (e.g., light; Smith

and Knapp 2001, Daehler 2003) that confer invasiveness. Buddleja davidii must

encounter the correct combination of moisture and warmth for germination and seedling

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. establishment. Propagule pressure (i.e., the composite measure of the number of

indivduals released and the number of release events into a region to which they are not

native; Lockwood et al. 2005) in combination with the availability of suitable habitat and

microsite conditions may account for successful colonization (Walker et al. 2006).

Buddleja davidii plants have been reported to retain seed on the plant over winter

(Miller 1984). Seed retention during unfavorable dispersal periods may be ideal for

wind-dispersed species in wet environments, especially for species such as B. davidii that

have no primary dormancy mechanism (Miller 1984). If seeds are only released when

they are capable of becoming airborne, the area of dispersal may be increased (Miller

1984). Furthermore, seed retention on the parent plant reduces the chance of dispersal

immediately before or during unfavorable winter conditions.

Nitrogen (N) and water are important resources for plants. Invasive species,

especially in dry and infertile environments, can increase invasivenss by increasing N-

and water-utilization efficiencies (Feng et al. 2007). Several ecophysiological

characteristics have been identified that facilitate B. davidii invasiveness in infertile

environments. Buddleja davidii leaves are high in N and phosphorus (P) concentrations

relative to other woody species (Comelissen et al. 1996, Bellingham et al. 2005, Feng et

al. 2007, Thomas 2007). A characteristic common to many woody colonizers, including

B. davidii, is the ability to assimilate nitrate (i.e., process through which inorganic N is

converted to ammonia and then to organic N) in their leaves rather than in roots or stems

(Al Gharbi and Hipkin 1984). Buddleja davidii allocated more leaf N to photosynthesis

than did the native woody species studied (i.e., Berberis vulgaris L., Cornus sanguinea,

Sambucus nigra, Crataegus monogyna Jacq. and Betualapendula Roth; Feng et al..

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 2007) and therefore, B. davidii had a higher resource capture ability (i.e., light-saturated

photosynthetic rate, maximum carboxylation rate, maximum electron transport rate) and

utilization efficiency (i.e., photosynthetic nitrogen utilization efficiency, maximum

electron transport rate) than did the natives. In addition, B. davidii demonstrated high

plasticity in photosynthetic use efficiency along an altitudinal gradient. This suggests

that B. davidii is able to adjust photosynthetie capacity over a wide range of

environmental conditions (Shi et al. 2006).

Buddleja davidii is a semi-deciduous species. Plants are able to remobilize N from

older leaves without a contribution of N from woody tissue (Thomas 2007). This

suggests that the N needed for new growth must be supplied from older leaves before leaf

abscission, especially in habitats where soil N is limited (Thomas 2007). The more N

remobilized from older leaves means there should be less N in leaf litter. The

contribution of N to the soil from the bi-annual loss of foliage from B. davidii is

unknown. Phosphorus remobilization patterns in leaves have not been determined. If P

is efficiently remobilized to new leaves than the concentration of P in leaf litter may be

low as well.

Buddleja davidii seedling specific leaf area (SLA) was high in a comparison of 80

woody species from the United Kingdon and North Spain (SLA mean ± SE 52.44 ±1.77

mm^ mg ’, n = 36;Comelissen et al. 1996). As B. davidii matures, SLA increases in

comparison to other woody species (Feng et al. 2007, Thomas 2007). This finding is

consistent with the results of Daehler (2003) who found that the invasive species he

studied had significantly higher SLA than native species.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Buddleja davidii seedlings that are greater than 4 weeks old are reported to be drought

tolerant (Miller 1984). Crystals have ben noted to form on the leaves. These crystals

may aid drought resistance and salinity tolerance (Miller 1984). Buddleja davidii was

more likely to be found on dry riverbank terraces than was the native Populus or Salix

spp. on the Tolt River, Washington (Leach 2007) This suggests that B. davidii may have

greater drought tolerance than the native riparian species studied (Leach 2007).

However, Leach (2007) suggested that B. davidii appeared to be less tolerant of frequent

and high intensity inundation than the two native species studied .

Herbivory

Buddleja davidii appears to be resistant to attack by most herbivorous insects in the

western world. This resistenance has been noted in the literature and has been attributed

to the production of defense compounds that are not common (Gillman 1998). Buddleja

davidii leaves are palatable to cattle and goats, but apparently not to deer (Gillman 1998).

In addition, leaves appear to be palatable to slugs, snails and other polyphagous insects

such as the aphids {Myzus persicae), the red spider mites (Tetranychus urticae) and the

glass house whiteflies {Trileuroides vaprarinorum). In addition, leaves may be palatable

to certain oligophgous insect species (Miller 1984). A few specialized insects have been

found feeding on B. davidii, including the weevil Gymnaetron tetrum, a dipteran leaf

miner {Amaroumyza verbasci) and a leaf bug (Campylomna verbasci).

Buddleja davidii has apparently evolved strategies to survive defoliation. Partially

defoliated B. davidii plants were able to increase leaf size, accelerate node productivity,

and increase longevity of new leaves. The impact of defoliation on the overall fitness of

B. davidii may be less significant in the short-term (Thomas 2007). However,

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. physiological mechanisms of compensation may decrease over time if the defoliation

continues, and this suggests that herbivory may be an effective means of biocontrol over

the long-term (Thomas 2007).

Buddleja davidii demonstrates little susceptibility to disease; however, some cultivars

carry cucumber mosaic virus, alfalfa mosaic, or tomato ringspot virus. These viruses

could negatively affect the horticultural industry (Eric and Grbelja 1985, Hughes and

Scott 2003, Perkins 1991). Viral infections such as these reduce plant vigor and

adaptability and provide a source for cross-contamination of landscape plants or crops.

When viruses are eliminated during tissue culture, plant health can be improved (Perkins

and Hicks 1989, Duron and Morand 1978). Cultivars of the genus Buddleja in Europe

suffer from apical diebaek, a disorder that reduces plant quality. Micropropagation

techniques are currently being developed that eliminate infections that decrease the

health of stock plants (Phalan et al. 2005).

Human Ecology of Buddleja davidii

Medicinal Uses

Widespread sources indicate that certain species of Buddleja have been used for

centuries as folk medicine for a variety of ills such as cancer, snakebit, infections,

hemorrhage, cardiac disease, kidney disorders, sedative effects, digestive disorders,

arthritis and rheumatism and skin and respiratory conditions (Norman 2000).

Nevertheless, various Buddleja species have played a relatively minor role in traditional

medicine (Houghton 1984, Houghton et al. 2003). Several types of chemical compounds

have been isolated from plants, including flavonoids (i.e., secondary metabolites that

produce pigments and are associated with protection from microbes and insects) and

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. other shikimate-derived compounds (i.e., the common aromatic biosynthetic pathway;

Houghton et al. 2003, Sprenger 2007). Leaves of certain species o îBuddleja have been

used for centuries in China for fishing because they are known to kill fish. Three

glycosides, eatalpol, methylcatalpol and aucubin, were been found initially by Duff and

others (1965). This work on toxic compounds found in the genus Buddelja was later

expanded on by Houghton and others (2003). Additionally, five novel toxic

sesquiterpenes (buddledin A, B, C, D and E) have been isolated from the root bark.

These sesquiterpenens are thought to be piscicidal agents (i.e., toxic to fish). These toxic

compounds may also have deterrent effects on potential herbivores.

Horticulture and Butterfly Enthusiasts

Buddleja davidii is a widely cultivated and popular garden plant of economic value to

the horticultural industry (Turnbull 2004, Wilson et al. 2004a). Certain B. davidii

cultivars were worth over $200,000 per year to Georgia, USA, plant growers (Dirr

1997). To growers outside of Georgia, plants were worth over $1,000,000 armually

(CANR 1998). Oregon exports approximately 66% of its Buddleja davidii nursery crops

to other states and Canadian provinces outside of the Pacific Northwest (Ream 2006)

In addition to the aesthetic and fragrant appearance of B. davidii, the flowering shrub

has been closely linked with butterflies, moths, and hummingbirds. Butterflies (Order

Lepidoptera) observed visiting B. davidii include the Peacock butterfly (Inachis io), the

Marbled white butterfly (Melanargia galathea), the Eastern comma butterfly (Polygonia

comma), the Monarch butterfly {Danaus plexippus) and several Swallowtail butterflies,

including the Common, Eastern tiger and Spicebrush butterflies {Papilio machaon, P.

glaucus, P. troilus). Sachem (Atalopedes campestris). Silver-spotted skipper (Epargyreus

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. clams) and Painted lady {Vanessa carduv, Giuliano et al., 2004; Stuart 2006). Also,

many other types of wildlife are attracted to the clear, sugary nectar of B. davidii flowers.

Moths (including the hummingbird hawk-moth {Macroglossum stellatrum), broad-

bordered bee hawk-moth {Hemaris fuciformis), wasps, hornets, lacewings and beetles

have all been noted as visitors to B. davidii flowers (Stuart 2006). In the New World,

Hummingbirds (Trochilidae) have been observed to visit gardens with B. davidii

(Pickens 1931, Stuart 2006).

Bruner (2005) found that B. davidii were visited by native butterflies more than five

other Buddleja species. Giuliano and others (2004) studied plant preference by

Lepidopteran species, and found that Lepidopteran in urban parks in New York City used

(i.e., as a food source and resting area) B. davidii more than other plants in the same

vicinity.

Policy

Human activity is an increasingly important mechanism of plant dispersal (Hodkinson

and Thompson 1997). Gardening is a worldwide recreational pastime that has

contributed to the spread of many plants species around the globe (Thacker 1979,

Hodkinson and Thompson 1997, Reichard and Hamilton 1997, Reichard and White

2001). In particular, the horticultural trade has been recognized as one of the main

pathways for plant invasions (Dehnen-Schmutz et al. 2007).

Naturalized B. davidii is considered by some problematic because it may potentially

out-compete native, agricultural, and silvicultural taxa. It readily out-competes plantation

pine species and thus, could have an economic impact on the pine silviculture industry

(Richardson et al. 1996). Buddleja davidii eolonizes abandoned areas and is eonsidered

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. an urban invasive (Reinhardt et al. 2003). Transportation routes have been negatively

affected by naturalized B. davidii in Europe (Reinhardt et al. 2003, Blacker 2006).

Buddleja davidii was listed as noxious in 1973, 1993 and 2000 by the New Zealand

Ministry of Agriculture and Forestry and cannot be propagated, released, displayed or

sold under the Biosecurity Act Sections 52 and 53 (NZ MAF 2007). In the Blue

Mountains of Australia, the species has been listed as a bush invader (Weeds of Blue

Mountain Bushland 2007). However, B. davidii has not yet recognized as a weed of

national significance in other areas of Australia even though congeners B. asiatica and B.

dysophylla have (Weeds Australia, 2007).

In the United States B. davidii is currently listed as a “B” designated noxious weed by

the Oregon Department of Agriculture (ODA). The species is on the invasive species

prohibited plant list in Eugene, Oregon and is listed as a Class B noxious weed by the

Washington State Noxious Weed Control Board (USDA 2007 WSNWB 2007). The

California Invasive Pest Plant Council (Cal-IPC) has evaluated B. davidii but it has yet to

be listed (CALFLORA 2007). The species is a category 3 watch species in the New

York metropolitan region (Brooklyn Botanic Garden 2007). The US EPA Green

Landscaping:Greenacres and U.S. Fish and Wildlife Service BaySeapes programs

specifically identified B. davidii as an ornamental that should no longer included when

landscaping (USFWS 2007, Welker and Green 2007).

Leach (2007) and Ream (2006) reported that B. davidii has invaded riparian areas in

Oregon and Washington, and has replaced riparian native Salix spp. and Populus spp.

Buddleja davidii encroachment along riparian corridors may affect salmon spawning

habitat (H. Turnbull, pers. comm.). Although gardens have been identified as the primary

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. source of invasive B. davidii seedlings in Oregon (67%), production nurseries contributed

seedlings as well (Ream 2006). Furthermore, plants sold by the nurseries probably

increase the amount of seeds that can disperse to wildlands in Oregon. Efforts to curtail

the spread of B. davidii in Oregon prove ineffective because only B. davidii was elevated

to the noxious weed quarantine list in 2004. None of the cultivars were included on the

list.. All B. davidii sold in Oregon are of named cultivated varieties, such as “Black

Knight” and “White Profusion,” and thus, are exempt from regulation (Ream 2006). The

cultivars are fertile members of the species and are capable of setting seed. Seed

dispersal from cultivars is evident because white flowers have appeared in the wild in

places that once only had the common lilac and purple varieties (Stuart 2006).

In Canada, B. davidii has invaded Garry Oak ecosystems (Craig and McCoy 2005)

and has been included as an “alien” species on Canadian plant lists (Haber 1996a-b 1995,

Lomer et al. 2002). However, is not been legally designated as a noxious species. Since

the time the species was introduced to Germany in 1900, B. davidii has become one of

the most common opportunistic plants (Bonsel et al. 2000, Reinhardt et al. 2003).

Buddleja davidii is considered one of the top 20 weeds in western Europe (Sheppard et al.

2006).

On the other hand, efforts by the Keep Croxley Green group (KCGG) in the United

Kingdom have resulted in the Development Control Committee of Hertsfordshire

registering a B. davidii field as a “Village Green” and thus guaranteeing its protection

from destruction in perpetuity (KCGG 2008). A quarry that was later used as an asbestos

waste dumping area after mining was abandoned, now has naturalized thickets of B.

davidii that are valued for beauty and wildlife (i.e., butterflies, birds, grass snakes, foxes.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. bats and badgers) attraction (Doughty 2007, FCGG 2007). According to the Countryside

and Rights of Way Act of 2000 (MOJ 2008), any plant, shrub or tree, of whatever origin,

is assigned as a natural feature of the protected landscape. Therefore, the aet protects

native and non-indigenous speeies from destruction. The consequence of protecting an

invasive non-indigenous plant speeies in this case can be debated. However, efforts to

control B. davidii, should it prove to be invasive and problematic, would be hampered by

legal protection.

Management

Land managers are tasked with the conservation and preservation of wild lands. This

often involves rehabilitating areas that are infested with invasive non-indigenous plant

species. Several methods are available (Reichard 1996, Reinhardt et al. 2003, Ream

2006). Mechanical, physical, or combined mechanical and physical methods have had

mixed results in controlling B. davidii. Dead-heading (removing seed capsules before

they ripen) is recommended to reduce the spread of seeds (Savonen 2004, Turnbull 2004,

Ream 2006). Yet many gardeners are reluctant to deadhead because it reduces the

quality of the shrub in subsequent years. Deadheading also increases the plant’s

susceptibility to disease (Warr et al. 2002).

Physical removal on a small spatial scale may help in the early stages of invasion.

Young shrubs can be dug up, although this method is not recommended for mature plants

in well established populations. Cut plants should be treated with glyphosate herbicides

(Kaufman and Kaufman 2007). Small-scale eradication efforts may be successful;

however, the removal efforts can be so damaging that they change the habitat so it is no

longer suitable for desired species and again susceptible to reinvasion (Myers et al. 2000,

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Zavaketa et al. 2001). Buddleja davidii removal sites should be replanted with native

species and monitored for regrowth of B. davidii.

Glyphosate herbicides without surfactants were effective against small shrubs in

Oregon (Ream 2004). Large shrubs that have heavy pubescence were somewhat less

vulnerable to foliar application. Treatment with triclopyr or imazapyr did not appear to

be effective, and there was concern about the negative consequences to native plants and

invertebrates potentially impacted by spraying these herbicides (Ream 2006). Directed

and precise application, such as painting cut stumps, was effective, but more labor

intensive and costly than spraying. Additionally, Ream (2006) noted that some seeds

appeared to have matured on the herbicide treated plants. Zazirska and Altland (2006)

prefer cutting and painting over the direct spraying method. The nature of cutting and

painting removes all flowers and seeds; therefore, if cut stems are removed from site,

seed maturation and dispersal are not of concern. Care must be taken in removing B.

davidii debris because stem and root fragments readily regenerate. Debris piles that are

not burned, composted, or otherwise treated in such a way to kill all seeds and stems and

root fragments can become a concentrated source of plantsi in the next season.

New Zealand has employed the natural herbivores of B. davidii in the treatment of

this invasive plant (Kay and Smale, 1990, Watt et al. 2004, in press). Laboratory testing

of Cleoptus japonicus indicated that grazing by the C. japonicus weevil had a substantial

negative effect on B. davidii growth (Brockerhoff et al. 1999, Thomas 2007). A first

evaluation of C. japonicus, which was released in New Zealand in 2006, showed a

damage intensity of about 60% defoliation on plants within the release area (Thomas

2007). However, it is difficult to predict future defoliation patterns and impact on the

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. New Zealand B. davidii populations because the genetic adaptations of either B. davidii

or the insects may eventually shift or nullify the interaction.

Sterile cultivars are being developed to allow the continued presence of B. davidii in

gardens, and curtail invasiveness (Pellet 2006). The B. davidii breeding program at the

University of Arkansas has been sueeessful in developing a sterile B. davidii hybrid to

replace the invasive varieties (Lindstorm et al. 2002). Sterile strains may extend B.

davidii flowering time because resources may be no longer shunted to fruit and seed

production. This could, in turn increase the tree’s attractiveness to butterflies. Bruner

(2006) speculates that B. davidii’s attractiveness to butterflies could be enhanced further

if sterility could be achieved without disrupting normal nectar production.

Conclusion

Prolific seed production, a short juvenile period, aggressive growth rates, and a wide

range of tolerances to various environmental conditions are several of a suite of traits

shared by plant species bred for hortieulture. Invasive plant species share these same

qualities (Reichard 1997, Rejmànek and Richardson 1996, Rejmànek 1999, Moller 2003,

Wilson et al. 2004b). These same eharacters allow B. davidii to readily colonize disturbed

sites. Extremely low temperatures (< 28.8 °C), drought (most likely for seedlings only)

and low-light levels (shade) appear to be the only known factors that limit B. davidii’s

distribution wordlwide. Consequently, the species is found primarily in frequently

disturbed, open, lightly-vegetated areas such as abandoned urban areas, road and railroad

edges, forest elearcuts and natural floodplains. Buddleja davidii establishment is likely in

or near anthropogenieally manipulated landscapes such as agricultural fields and gardens.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Whether the species’ distribution has been limited by dispersal barriers or environmental

limits has not yet been determined. The potential future distribution of B. davidii has not

been predicted either.

Buddleja davidii is difficult to remove or manage once it has established in a

disturbed area. Manual removal is laborious and costly. Pesticides are effective in small

areas in the short term, but must be applied manually and repeatedly. Biocontrol methods

currently being used in New Zealand may prove effective. However, the deliberate

introduction of another non-indigenous species (i.e., the biocontrol agent itself) to an

ecosystem is sometimes considered too risky to be eonsidered (Sheppard et al. 2005).

In the absence of disturbance, natural plant succession may lead to the elimination ofB.

davidii. However, B. davidii, by nature, establishes on frequently disturbed sites which

provide source for satellite populations that can repopulate new and post-disturbance

landscapes. Because it is well known that species invasion via multiple loci is the most

effective means of establishing non-indigenous species in a new environment (Mack et

al. 2000), the continued presence of non-sterile B. davidii cultivars in urban, residential,

and wild areas guarantees continued réintroduction into native areas (regardless of native

control efforts).

Despite the potential for B. davidii to usurp native speeies, gardeners and

horticulturalists continue to enjoy this beautiful and fragrant shrub. Buddleja davidii is

much appreciated by many for its beauty and attractiveness. Furthermore the continued

sale of the plant economically benefits the horticulture and nursery trades. This leads to

the conundrum of whether to implement policies to limit the spread of B. davidii and

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. curtail current distribution, to continue to promote its presence, or to develop means that

best satisfy both desires.

What is not often acknowledged in the ecological study of biological invasions is the

anthropogenic cultural and emotional dimensions that drive land management strategies

(Kendle and Rose 2000). When a speeies is pleasing to the public, regardless of its

origins, the public becomes the champion who advocates for the sepcies protection and

propagation. Buddleja davidii’s post-World War II establishment onto urban debris in

Europe may have added an explosion of color and thus, transformed ravaged landscapes.

Perhaps the passion expressed by Europeans for B. davidii is inadvertently linked to their

appreciation for the beauty that followed such a dark and violent period in history. Even

if methods were found for the efficient removal of B. davidii, it seems unlikely that the

European public would condone such actions. As with the case of the now protected B.

davidii field in Croxley Green, removing this non-indigenous plant species in the Croxley

Green is no longer an option (even if removal were feasible). Ecologists must continue to

examine the impacts B. davidii has on natural ecosystems in order to promote informed,

rather than emotional, decisions.

In summary, ornamental plant species are often at the top of invasive species lists

(Reichard and Campbell 1996, Leland 2005, Dehnen-Schmultz et al 2007). Many

“charismatic” plant species (i.e., popular garden shrubs and trees) have naturalized their

way into the public’s emotional landscape (Culley and Hardiman 2007). It is unlikely

that management strategies that include eradication of these “charismatic species” will be

successful either logistically or culturally. The repercussions of B. davidii naturalization

are unknown. Therefore, further ecological research is needed to determine the long-term

Reproduced witfi permission of tfie copyrigfit owner. Furtfier reproduction profiibited witfiout permission. impacts to native ecosystems and landscapes inhabited by B. davidit and to predict the

ecological consequences of the subsequent continued réintroduction of B. davidii. We

also must consider the relationship that humans have with B. davidii as well.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Figure 1. Illustration of Buddleja davidii Franchet (1) flowering branch, (2) flower, (3) pistil, (4) open corolla, (5) fruit and (6) seed (Illustrator: P. Grossman).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Native Range Buddleja davidii

Xinjiang an SI

laamii an SSII Sichuan lanæa ipejiang nizlrai

uangiof Guanguong

Beijing

] 250500 1,000

Kilom eters

Figure 2. The native range (provinces) of Buddleja davidii in China are shown in gray.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. p co o n (D } • rlü '#.-0ü o :s cs S| I1 1 00 ü f p I |§ f . Pj I gc3 s O il Io IS'S u I il W lîo (Nii « ÎP " - r % .1 E I ùC ë - ë %u I o GJ fi 10 I a I I en â 0 oo O o \ §

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. B 0 1 D MOB o c a

not to scale.

Figure 4. Distribution of naturalize Buddleja davidii in North America. The shaded states and provinces in the United States and Canada are locations where naturalized Buddleja davidii has been recorded as naturalized by NatureServe (2007) and other additional sources; California (Roja 1998, CALFLORA 2007), Connecticut, Georgia, Hawaii (Sharmon and Wagner 1996, Wagner et al. 1999, Starr et al. 2003), Kentucky (Gunn 1959), Maryland, Massachusetts, Michigan, New Jersey, New York (Stalter and Lamont 2002), North Carolina (Mellicamp et al. 1987), Ohio, Oregon (Ream 2005); Pennsylvania, South Carolina (Mellicamp et al. 1987), Tennessee (Watch List A 2007), Virginia, Washington (Collette and Naiman 1994, Leach 2007), West Virginia (PLANTS 2007) and British Columbia and Ontario, Canada (Craig and McCoy 2005). Although not shown, it has also been found in Alabama (Clark 1971) and Puerto Rico (Starr et al. 2003).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 68

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. __ k^ÂK*»

■ : " ' t #

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 3

SUCCESSION ON NEW ZEALAND FLOODPLAINS

DOMINATED BY AN INVASIVE SHRUB,

BUDDLEJA DAVIDII

Abstract

Invasive species that displace native species may impact key biotic interactions and

ecosystem properties. Bellingham and colleagues (2005) determined that Buddleja

davidii, an invasive shrub, dominated the Kowhai River floodplain. South Island, New

Zealand, accumulated phosphorus and increased soil nitrogen and phosphorus. These

soil nutrient changes may eventually alter plant successional trajectories. Plant

community composition, B. davidii foliar nutrient concentrations and soil properties and

chemistry were measured on on 9-m^ plots designed to represent a four-stage

developmental (i.e., open, young, vigorous and mature) chronosequence (i.e., time since

last disturbance by flood) on 5.£/ovi£///-dominated floodplains. Seven South Island

catchments were characterized by the coast on which they were located and type of

waterway. The successional development of the B. davidii-àominateà communities

progressed from flood to native and non-indigenous forbs and grasses to woody shrubs

and trees. However, B. davidii cover was often 20 times greater than that of any other

species, native or non-indigenous. Only twenty-three of the 282 floodplain resident plant

species, both native and non-indigenous contributed more than an average of 3% of the

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. total vegetative eover. Several native forbs and grasses typieally found on floodplains

not invaded by B. davidii, were present in low frequencies (< 2%) and had low cover (<

3%). Buddleja davidii dominated the open, young and vigorous developmental stages (0

- 8 yrs after flooding) on exposed floodplains, elevated channel islands and on the edges

of riparian terraces habitat. After this time, the species declined in frequence and cover.

Buddleja davidii plants greater than 10 yrs old were about seven times less likely to be

found on the floodplains than younger individuals. The older individuals were restricted

to the edges of riparian terraces. Native shrubs and trees were present in all four stages

as seedlings, saplings and adults yet in low frequencies and had an average cover of <

3%. An exception was Coriaria arborea, which was found at 20% of plots and had an

average cover of 37.5 ± SE 2.73%. There was a four-fold increase in B. davidii foliar

nitrogen and phosphorus concentrations along the developmental gradient that stabilized

in the later stages. Soil physical properties did not vary between stages or catchments;

however soil phosphorus and nitrogen concentrations were positively correlated with B.

davidii biomass. This suggests that B. davidii may augment soil fertility. These results

were consistent with Bellingham and others (2005) and demonstrate that B. davidii can

alter successional dynamics by dominating the plant community, out competing native

species and enhancing soil fertility.

Introduction

The general patterns of plant succession are well understood (Whittaker 1975, Glenn-

Lewin and van der Maarel 1992). In any environment there is a characteristic sequence

of biotic communities that successively occupy and replace each other over time

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. following disturbance. Sequential changes occur in the abiotic and biotic components of

successional ecosystems as they develop with a certain degree of predictability (Connell

and Slatyer 1977, McCook 1994).

In general, light levels are high when plant biomass is lacking immediately after

floods scour and remove most of the biotic component from above- and below-ground

communities on floodplains (Fig. 7). Although the propagule pool will ultimately

determine species richness, the numbers of species increase sharply in the open and

young stages before the total numbers of species eventually plateaus (Fig. 7). The initial

rate of biomass accumulation will be relatively rapid, yet over time the rate will decrease

through self-thinning and senescence (Fig. 7).

The plant community composition usually transitions from forbs to grasses towoody

shrubs to trees and depends on the availability of propagules (Thompson et al. 1997,

Lockwood et al. 2005), suitable germination microsites (Walker et al. 2006), above- and

below-ground resource availability (Wardle 2002), the presence or absence of mutualistic

symbionts (Grime 2001; Fumanal ct al. 2006) and interactions among resident plant

species (Callaway and Walker 1997). The outcome of these interactions will determine

which species will, throughout succession, establish, reproduce, and spread (McCook,

1994). Non-indigenous plant species have often replaced the native pioneers that

colonize denuded floodplains. These species may change ecosystems processes

(Richardson et al. 2007) and alter the rate of successional trajectories (Kota et al. 2006).

Floodplains are disturbance-dominated ecosystems characterized by a high level of

habitat heterogeneity and have a diverse biota adapted to the high spatio-temporal

heterogeneity (Tockner and Stanford 2002). Floodplain plant succession is closely tied to

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. high intensity floods that alter the geomorphology and path of the active channel and

reset successional processes (Hughes 1997, Gray and Harding 2007). The expansion and

contraction of suitable surfaces for vegetation establishment (Tockner and Stanford 2002)

leads to an intergraded mosaic of species and vegetation types the establishment of which

is determined by each species’ tolerance of microsite conditions (Walker et al. 2007).

The native plants species that establish on New Zealand river floodplains are relatively

predictable (Cockayne 1927, Calder 1961, Williams 1979, Smale 1990, Wardle 1991,

Gibb 1994, Bellingham et al. 2005). Dicot forbs (e.g., Raoulia spp.), tussock grasses

(e.g. Cortaderia richardii), woody shrubs (e.g., Coriaria arborea) and trees (e.g., Kunzea

ericoides; Fig. 8) may establish in series or simulaneously. The timing and order in

which the species are introduced and the longevity of the individuals are rarely static.

Floodplains that have not been exposed to non-indigenous species generally have

lower plant biomass and less structural diversity than floodplain communities that that

have been invaded by non-indigenous plants (Wardle 1991, Gibb 1994, Williams and

Wiser 2004). When floods are infrequent native biomass and structural diversity

evcntally increase. Yet biomass and diversity of the mature native community wanes in

comparison with the vegetative community dominated by non-indigenous species. When

invasives have more biomass than the co-occurring natives the invaders will sequester

nutrients, increase litter and disrupt nutrient recycling (Ehrenfeld 2004).

Buddleja davidii (family Buddlejaceae), an invasive woody shrub native to China has

naturalized in New Zealand (Chapter 2). Williams (1979) and Smale (1990) found B.

davidii quickly displaced primary native colonizers, including both herbaceous (e.g.,

Epilobium spp., Roualia spp.) and woody (e.g., Kunzea ericoides, Pseudopanax spp.)

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. species on floodplains in Urewera National Park, North Island, New Zealand. They

concluded that naturalized short-lived B. davidii accelerated floodplain succession by

displacing the longer-lived native species (e.g., Kunzea encodes).

Bellingham and colleagues used a four-stage developmental chronosequence of time

since last flood to study the impact of B. davidii on the Kowhai River, South Island, New

Zealand (Bellingham et al. 2005). They defined the stages as: 1) “open” (mostly

unvegetated; seedlings <0.5 m tall), 2) “young” (plant canopy had not coalesced; plants

0.5-2 m tall), 3) “vigorous” (complete plant canopy cover; plants 2-4 m tall), and 4)

“mature” (closed plant canopy; some senescing individuals; plants > 4 m tall; Bellingham

et al., 2005). The assumption was that each developmental stage of the floodplain plant

community would have repeated the successional sequence of every other older stage up

to its present age.

Buddleja davidii overwhelmingly dominated (>50% cover) the open developmental

stage of the floodplain of the Kowhai River, South Island, New Zealand while the young,

vigorous and mature stages covered < 15% of the floodplain (Bellingham et al. 2005).

There was a 8-fold decline in the presence of B. davidii in the mature stage compared to

the open stages (Bellingham et al.. 2005). Conversely, the presence of the native

Coriaria arborea increased in the mature stages. These results suggested that although

B. davidii was an aggressive colonizer the native species eventually regained dominance

in later stages (Bellingham et al. 2005).

Bellingham and colleagues also determined that B. davidii had several novel impacts

on soil nutrients, specifically the plant accumulated P and the increased the

concentrations of soil N along the four-stage developmental chronosequence (Bellingham

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. et al. 2005). The aecumulation of P in the soil is linked to the recent determination that

B. davidii is mycotrophic (Dickie et al. 2007) and therefore an efficient P scavenger. If

Stored P is not remobilized before leaf abscission then B. davidii foliar litter should enrich

understory soils. The progressive increase in soil N was explained by Bellingham and

others (2005) by the increased biomass of C. arborea, a N-fixer (i.e., has symbiotic, N-

fixing bacteria in its root nodules). However, B. davidii foliage is relatively high in N in

comparison with other woody shrubs and trees and therefore may contribute to soil

fertility (Al Gharbi and Hipkin 1984, Bellingham et al. 2005, Feng et al. 2007, Thomas

2007).

The novel impacts of B. davidii, particularly its ability to dominate the plant

community, displace native plant speeies and alterate soil fertility have important

community- and ecosystem-level implications for plant successional dynamies

(Bellingham et al. 2005). In order to determine whether these processes were evident on

other B. davidii-(lom\x\a.ieA floodplains, I studied the plant community and soil properties

and chemistry of B. davidii stands representive of a four-stage developmental (i.e.,open,

young, vigorous and mature) chronosequence (i.e., time since disturbance by flooding) on

floodplains in seven catchments on the South Island, New Zealand. I asked the following

three questions; (1) Does B. davidii dominate early and decline later in the successional

sequence on other floodplains as it did on the Kowhai River floodplain? (2) What are the

floristic and ecosystem components of B. davidii stands over time on other floodplains?

(3) Does B. davidii impart the same novel impacts on soil N and P on other floodplains as

in the Kowhai River floodplain?

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Methods and Statistical Analysis

Study sites

Field reconnaissance of floodplain invaded by B. davidii (identified from a search of

records from New Zealand herbaria collections, the Department of Conservation invasive

species database and the National Vegetative Survey database) determined the eight

floodplains in seven New Zealand catchments to be included in this study (Fig. 9, Table

1). Henceforth catchments will be referred to in the order of their geographic location

from the NW, SW, NE to SE. These catchments were selected because of the presence of

plant communities dominated by B. davidii that represent a four-stage developmental

chronosequence (i.e., time since last disturbance by flood; Fig. 10). Plant communities of

the following stages were designated as; 1) “open” or ‘a’ (mostly unvegetated with B.

davidii seedlings <0.5 m tall), 2) “young” or ‘b’ (plant community canopy had not

coalesced; B. davidii plants 0.5-2 m tall), 3) “vigorous” or “c” (plant community had

coalesced; B. davidii plants 2-4 m tall), and 4) “mature” or ‘d’ (plant community has

coalesced; some senescing B. davidii individuals; dominant plants > 4 m tall; Bellingham

et al. 2005). The chronosequence or space for time substitution method infers a time

sequence of development from a series of plant communities differing in age since a

flood removed all vegetation from the plant communities (Pickett 1988, Johnson and

Miyanishi 2008). The assumption being that each plant community in the sequence

differs only in age and that each plant community has the same history (Johnson and

Miyanishi 2008). If the assumptions are correct, than each site will have repeated the

successional sequence of every other older site up to its present age.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. There was one river or creek per catchment, except for the Porarari. Two creeks,

located within 5 km of each other with similar geology, hydrology, adjacent land use and

B. davidii density, were sampled in the Porarari catchment. This enabled an adequate

number of replicates of the developmental stages in all catchments.

Four of the catchments that were selected are located on the West Coast of the South

Island (Fig. 9). The Mokihinui River drains the Mokihinui River catchment. The

headwaters of the Mokihinui catchment are located in the Glasgow Range. Nine B.

£/avi(//i-dominated plots were established on the floodplain of the Mokihinui River < 5

km from where it drains into the Tasman Sea. The number of replicate plots of each

stage (i.e., a, b, c, d; Fig. 10) are shown on Figure 9. The populations of the communities

nearest where measurements were collected, Mokihinui and Summerlea, are 162 and 72,

respectively. State Highway 67 crosses the river west of the the town of Mokihinui. The

catchment is a large inland basin of almost wholly unmodified native forest.

South of the Mokinhinui catchment and west of the Paparoa Mountain Range is the

Porarari catchment. Fagan and Baker Creeks are two < 6 km creeks. The head waters of

Fagan Creek is Mt. Royall and Baker Creek is Mt. St. Patrick. Five plots were

established on the floodplain of each of the creeks. The dominant land cover in the

catchment is native forest. Land use in the catchment is limited by roughed terrain.

Sheep and cattle pastures are located adjacent to segments where the plots were

established on both creeks. State Highway 6 crosses both creeks < 1 km form where they

drain into the Tasmin Sea. Barrytown (pop. 192) is the community nearest to the two

creeks.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. The Arnold River catchment was the most inland South Island catchment included in

this study. The catchment is located on the western fringe of the Southern Alps. Ten B.

rfov/c/ü-dominated plots were established on Camp Creek floodplain. The creek is < 7

km. Camp Creek drains a section of the Alexander Mountain Range. The dominant land

cover in the catchment is native forest. Sheep and cattle pastures are adjacent to the

segment of the creek dominated by B. davidii. Inchbonnie is the community nearest to

Camp Creek (pop. 166).

The most southern catchment included in this study was the Waiho River catchment.

The Waiho River catchment drains the Omoeroa Mountain Range. Eleven plots were

established on the Docherty Creek floodplain. Docherty creek is approximately 5 km

from the community of Franz Josef (pop. 320). The dominant land cover in the

catchment is native forest. The land use on the downstream segement of Docherty Creek

is limited pasture (i.e., sheep and cattle). Docherty Creek floodplain is used for

recreation (i.e., horseback riding, driving off-road and tramping) and gravel mining.

There were three East Coast catchments included in the study (Fig. 9). Twelve plots

were established on the Puhi Puhi River located in the Hapuku Catchment. The Puhi

Puhi is an actively migrating river that drains the northeastern end of the Seaward

Kaikoura Range. The rivers headwaters are located west of Mt. Alexander. The Puhi

Puhi River drains into the Hapuku River. The Hapuku catchment was the most densely

populated catchment included in this study. The Puhi Puhi River is 14 km from Kaikoura

(pop. 3,483). The dominant land cover at the headwaters is native alpine shrub and

forest. Land use adjacent to the downstream segment of the Puhi Puhi River is

predominantly sheep pastures and agriculture. Driving off-road, hunting, horseback

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. riding and tramping are several of the recreational activities conducted directly on the

floodplain.

Twelve plots were established on the Oaro River located in the Omihi catchment.

The catchement is on the southern end of the Seaward Kaikoura Mountain Range. The

Oaro River is a braided-river. The plots were established < 5 km from the community of

Oaro (pop. 81). The dominant landcover at the river’s headwaters is native forest while

the landcover adjacent to the downstream segment is cattle and sheep pasture and

agriculture.

The Conway River is in the Conway River catchment. The catchment is located

south of the community of Kaikoura. Ten plots were established < 2 km from where the

river drains into the Pacific Ocean 30 km south of Kaikoura. The Conway River runs for

30 km through the Hundalee Hills at the south end of the Seaward Kaikoura Mountains.

Highway 1, the primary East Coast highway, crosses all three of the East Coast

waterways. Catchment- and river attributes are provided in Table 3-1 and Appendix I.

Five to fifteen 3 x 3 m^ plots were established in plant communities that represented

the four developmental stages defined above (Fig. 10). The location of each plot in the

plant community was arbitrarily assigned without preconceived bias (McCune and Grace

2002; Fig. 11). The approximate age of the plant community was determined from the

average number of growth rings measured from three ramets cut at ground-level from B.

davidii plants typical of the actual plot (the individuals selected to age the community

were adjacent to the actual plot, not located in the plot). The final number of 3 x 3 m

plots in each catchment was based on the actual number of B. davidii plant communities

on the floodplain that conformed to the stages as described above (Fig. 10). The location

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. of the center of each plot (New Zealand Geodetic Datum 2000) was collected using a

global positioning system unit (Garmin eTrex, Garmin Ltd., Olanthe, KS, USA).

Vegetation and Soils

Between October 2004 and April 2005 all vascular plant species rooted within each

plot were identified and the percentage of all vegetative coverage of the tree (1 2 -5 m),

tree and shrub (5 -2 m), shrub (2 - 0.3 m) and understory (< 0.3 m) strata were estimated

using fixed cover classes (1 = < 1 %, 2 = 1-5%, 3 = 6 - 25%, 4 = 2 6- 50%, 5 = 51-

75%, 6 > 75%) and the height of all B. davidii >10 cm were measured. The

aboveground biomass of B. davidii was calculated for individual plants located within

each plot using an allometric relationship based on canopy area and aboveground

biomass (dry mass of leaves and stems). The equation was estimated from the height and

biomass of B. davidii individuals representing the full size range of individuals

encountered on the Kowhai (Bellingham et al., 2005) and Conway (unpublished data)

Rivers: B. davidii shoot mass (g) = -4.44 + 1.84 (natural log B. davidii height), n = 33,

r^=0 .88 , f <0.001.

Fully expanded leaves from the canopies of five B. davidii plants per each plot were

collected and dried at 35°C before being ground, subsampled and digested using the

semi-micro Kjeldahl method (Blakemore et al. 1987). Nitrogen (N) and phosphorus (P)

levels were determined colormetrically on a flow-injection analyzer (Landcare

Environmental Chemistry Laboratory - Method 204; Quikchem 8000; Lachat,

Milwaukee, MI, USA). Buddleja davidii voucher specimens, collected from each river,

were archived at the Allen Herbarium, Lincoln, New Zealand.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. In April 2005 digital hemispherical photographs taken 1 m above ground in the center

of each plot were acquired to determine total light transmission. The percentage

transmission of total light through the canopy was measured on the digital images using

Gap Light Analyzer 2.0 (Frazer et al. 1999).

Soils were sampled in all survey plots and analyzed for both physical and chemical

properties. Floodplain parent geology and dominant soil type classification were based

upon the Landcare Research Geospatial Data Integration Portal (NZ Soils Portal, 2008).

Depth of the entire organic layer (Ao horizon), where present, was determined at five

points within each plot. Physical properties were determined from soils sampled from a

pit (20 X 20 cm^ wide, 10 cm deep) adjacent to each plot. Volume and mass were

determined for each of three size fractions of inorganic particles (gravel, >16 mm

diameter; cinder, 2-16 mm diameter; and fines, <2 mm). After discarding any surface

litter, the entire organic layer (Ao horizon) and the top 10 cm of the mineral soil (Ai

horizon) were removed. The fractions were sieved and the volumes (by flotation) and

mass of gravel and cinder were determined. The mass and volume (by flotation) of the

fines were determined from the dried (40°C, 4 d) fraction brought back to the lab. The

fractions of sand (particle size = 0.06-1.00 mm), silt (0.002-0.06 mm) and clay (< 0.002

mm) were determined from the fines using soil hydrometer soil particle size analysis

(Tan 1996).

Mineral bulk density (A, horizon; g cm'^) was determined in two ways; the dry mass

of the fines per volume of fines and the dry mass of gravel, cinder and fines combined per

pit volume (total bulk density). The field capacity (a.k.a water holding capacity) of

mineral soils was determined by first saturating the soils, draining them for an hour and

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. then determining the difference in mass between wet sample and its mass after drying at

60°C for 4 days (Tan 1996).

Chemical properties of soils were analyzed on one composite sample (3 0.5-L, 10 cm

deep grab samples were composited from which 1 0.5-L subsample was taken) of mineral

soil ( A l horizon) per plot. Depths of surface litter and A q horizon were determined when

present. All chemical analyses were performed on sieved (2 mm mesh) dry soils

including pH (1:1 ratio of soil and distilled water), total N and organic carbon (C)

(Landcare Environmental Chemistry Laboratory - Method 114, LECO, St. Joseph, MI,

USA) and Olsen available P (Blakemore et al., 1987; Landcare Environmental Chemistry

Laboratory - Method 124; Quikchem 8000; Lachat, Milwaukee, MI, USA). Estimates of

soil N, C and P on an areal basis (g cm'^; i.e., estimates of how many grams of nutrients

might be found in m^ of the fines fraction of the mineral soil) were calculated by

multiplying the concentration of the nutrient (%) x soil bulk density x volume of the fines

(%) X soil volume (1 m^ by 10 cm depth).

Land-Cover Data

Vegetation and land-cover estimates of the catchments were obtained from Landcare

Research based upon the environmental classification of New Zealand Land

Environments of New Zealand (Leathwick et al. 2002). New Zealand census data was

taken from Statistics NZ (2006). Annual precipitation (mm yr ’; WRENZ 2007) for each

catchment was used to characterize climate and its likely influence on plant distribution

(Williams and Wiser 2004). An index of the density of human habitation in the

catchments was calculated from the log of the number of buildings ( 0, 1, 100, etc.:

Williams and Wiser 2005) shown on NZ map series 260 and 2.5 m resolution air

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. photographs (Maptoaster Topo New Zealand, Integrated Mapping Ltd. 2007) within each

catchment. Additional catchment and river data are provide in Appendix I.

Data Analvsis

A direct discriminant function analysis was performed using the three plot-level

variables as predictors of membership in the four groups. Predictors were B. davidii age

(i.e., number of B. davidii tree rings; see above), light transmission (%; see above) and

total B. davidii biomass (g m'^; see above). The groups were the four stage

developmental chronosequence of B. davidii (i.e., open, young, vigorous and mature; Fig.

10; Tabachniek and Fidell 1996, SAS Institute Inc., Cary, NC, USA).

Principal factor extraction (a.k.a principle components analysis) with varimax

rotation was performed using SAS PROG FACTOR on catchment-seale variables (i.e.,

precipitation, human density index (log transformed), catchment area (log transformed),

maximum catchment altitude (log transformed), river length (log transformed), average

bed width of river or creek (log transformed) and upstream area (log transformed)) for the

seven catchments to determine whether the data would form into coherent subgroups.

Principal components extraction was used prior to principle factors extraction to estimate

number of factors, presence of outliers, absence of multicollinearity and factorability of

the correlation matrices using SAS 9.1 (SAS Institute Inc., Cary, NC, USA). With a =

.001 as the cutoff level, no catchments were identified as outliers.

The two factors that accounted for the most variability among catchments, denoted as

Factor 1 and Factor 2 were the main effects in the general linear models (GLM) used to

compare the plant community, foliar chemistry, soil property and chemistry attributes

measured in the four-stage developmental chronosequence (SAS PROC GLM). Tukey

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. HSD a posteriori tests were used to tests differences among least square means. Data

were transformed per Box and Cox transformations (1964) or other methods as

appropriate (square root for species richness, [(360/2*7t)+ arcsine-square root] for %

exotics and % woody species, log for foliar N, the inverse of foliar P, the log areal soil N

(g m'^) * 4.97, [areal organic C ' - 1J/-1226.004, the log areal P * 0.027 , 1/square root

for bulk density) to meet the data assumption (i.e., normality, equal variances and

scaling). Outlier observations (P<0.05) and influential observations (i.e., cases where the

scaled measure of the change in the predicted value of that observation was > 2, referred

to as the Dffits statistic) were removed when transformation did not correct effects.

Residuals were plotted to confirm correction. Regression was used to determine the

significance of relationships among variables. All statistical analyses in this study were

performed using SAS 9.1 (SAS Institute Inc., Cary, NC, USA).

Results

Successional stage classification

Tests of dimensionality for the discriminant analysis, as shown in Table 3-2, indicate

that both the dimensions are statistically significant. Dimension 1 had a canonical

correlation between response variables and developmental stage of 0.96, whereas the

dimension 2 of the canonical correlation was lower (0.73). Table 3-3 presents the

standardized canonical coefficients for both dimensions. As shown in Figure 12, the first

discriminant dimension maximally separated the open and young (right clusters) from the

vigorous and mature (left clusters) stages. The second discriminant dimension

discriminates the open from the young and the vigorous from the mature stages.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. The loading matrix of correlations between predictors and discriminant functions, as

seen in Fig. 12, suggests that the best predictors for distinguishing between the

open/young and vigorous/mature stages (first function) is light transmission and thus

accounts for the division between the two early stages from the two later stages. The

mean light transmission of the open and young stages are closer in distance (97.3 and

79.1%) than the vigorous and mature stages (30.1 and 27.9%; Fig. 12).

In the second discriminant dimension the predictors, B. davidii age, and biomass,

further separate the groups. The average age in the open stage (2.8 yr) was further in

distance from the young (5.9 yr) than the young from the vigorous (5.3 yr). The distance

from the average age of the mature stage (8.4 yr.) further divides the groups. Buddleja

davidii biomass increased among the open (37.98 g m'^), young (149.73 g m'^) and

vigorous (864.27 g m'^), yet decreased in the mature stage (268.03 g m"^), and therefore,

accounted for the division beween groups (Fig. 12).

There was a positive relationship between age and light transmission, with r^(?o) =

0.37, P<0.01, indicating that, in general, as the plots aged there was less light transmitted

through the canopy. Buddleja davidii age accounts for 31% of the variation in B. davidii

biomass (Fig. 13). Data points corresponding to the developmental stage of B. davidii are

show using different markers (Fig. 13). Buddleja davidii biomass was greater in the

vigorous stage than in the mature stage because self-thinning in the understory and B.

davidii senescence curtailed continued biomass accumulation.

The stability of the classification procedure was checked by a cross-validation run

(SAS PROC DISCRIM; Tabachniek and Fidell 1996). Approximately 25% of the cases

were withheld from calculation of the classification functions for the stability check. For

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. the 75% of the cases from which the function was derived, there was a 99.0% correct

classification rate. For the cross-correlation cases, classification declines to 90.0%.

These results indicate a high degree of consistency in the classification scheme and a

random division between the open and young and between the vigorous and mature cases

in the cross-validation sample.

Regression was used to verify a positive relationship between B. davidii age and B.

davidii biomass linear regression. Individual ANOVAs of the effect of catchment on the

three variables by developmental stage were not significant at a < 0.004. Based upon

these analyses the a priori classifications of the actual plots as one of the four

developmental stages was accepted for further analysis.

Catchment Principle Factor Analvsis

Two factors were extracted that accounted for 84% of the total variability (Fig. 14).

The squared multiple correlations (SMCs) indicated that all factors were internally

consistent and well defined by the variables; the lowest of the SMCs for for factors was

0.48. Four variables did not load on Factor 1 and Factor 2 based on a cut off of 0.45 for

inclusion (Tabachniek and Fidell 1996). Factor 1 accounted for 55% of the variation and

was identified as “coast” (denoted as west (Fig. 14a) or east (Fig. 14b)) because the

attributes longitude (-0.95) and annual precipitation (0.94) loaded the heaviest (Fig. 14).

The annual precipitation of the West Coast of New Zealand is five-times greater than the

annual precipitation on the East Coast (Molloy 1998). Factor 2 accounted for 35% of the

variation and was identified as “river type” based on bed width (0.98) and river length

(0.87) which loaded most heavily. The waterways were split between migrating rivers

with somewhat wide floodplains that are usually not fully inundated through the year

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. (Fig. 14c) and creeks that are relatively narrow and have less floodplain habitat in

relation to the size of their active channels (Fig. 14d). For all statistical analysis the

catchments were characterized by the coast that they were located (Factor 1; Fig. 9) and

whether they were rivers or creeks (Factor 2; Table 3-1).

Plant community

The total flora encountered was 282 plant species and the nativity assignments

included 123 (43.2%) native, 114 (40.0%) non-indigenous species and 35 unknown

(Appendix II). Plants identified to genus were assigned as native or non-indigenous

(non). When the genus was apparent nativity was identified based upon the subset of

species in the floodplain, otherwise nativity was listed as unknown (15.8%; Appendix II).

The unidentified specimens were primarily (77%) grasses and forbs that measured < 0.3

m in height.

Total species numbers by catchment was 57 in the Mokihinui, 61 in the Porarari, 61

in the Arnold River, 50 in the Waiho, 79 in the Hapuku, 128 in the Omihi, and 67 in the

Conway (Appendix III). A total of 70 families were found; however, there were only 11

families with > five representatives comprising 67.16% of the flora. The top five

dominant families were Poaceae (15.7%), Asteraceae (14.6%), Rubiaceae ( 8 .6%),

Fabaceae (7.10%) and Scrophulariaceae (3.8%). These families are numerically

dominant in New Zealand flora as a whole (Wilton and Breitwieser 2000; Williams and

Wiser 2004).

Five species in addition to B. davidii, were found at all sites; the native shrub

Coriaria arborea and the non-indigenous grass Holcus lanatus and forbs, Hypochoeris

radicata. Prunella vulgaris and Trifolium repens (The authorities for all genera and

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. species are provided in Appendix II). These species accounted for less than 2% of all

species indentified. Forty-four % of the species identified to genus were found at only

one catchment (Appendix III) and only 12% of the species were found in all four stages

(Appendix IV).

Species richness did not vary significantly among successional stages (open = 177;

young =118, vigorous = 153, mature = 100), however, species richness was significantly

greater on the west coast than on the east coast. Factor 1 accounted for 30.3% of the

variability (Fig. 15; F;=10.42, P=0.0019). Note that one plot in the Omihi Catchment

was removed because it was identified as an outlier (Cooks Distance Test; Neter et al.

1998).

The Omihi catchment had the greatest number of non-indigenous species (35) and the

Arnold River had the least number of non-indigenous species (12; Fig. 16). The

percentage of non-indigenous species did not differ among stages (F 3 73 =1.76, P =

0.0954). The percentage varied significantly among catchments both by coast (Fig. 16(a),

east coast > west coast; F 1,73 =23.68, P<0.0001) and river type (Fig. 16(b), rivers >

creeks; Fi,73=28 .20, P<0.0001). Percentages of non-indigenous species that were

determined to be statistically infiuencial were identified in in the vigorous and mature

stages in the Arnold and Omihi catchments apd were removed. Analytically there were

significant coast x stage (F3=3.66,P=0.0170) and river type x stage (F3=3.58, P=0.0187)

interactions. However, the contribution of each interaction to the sum of squares was

negligible and they were not considered in the interpretation of the data.

In addition to B. davidii (frequency 4; mean and SE cover 10.38 ± 9.06%; henceforth

the frequency or number of plots where the individual species was found and the mean

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. and standard error of estimated cover will be presents as frequency, mean and SE %

cover), four species of trees between 12 and 5 m were found. Two were native, Coriaria

arborea (1, 37.5%) and Kunzea ericoides (3, 13.67 ± 11.94%) and two were non-

indigenous, Racosperma dealbata (1, 15%) and Salix fragilis (1, 3%). All five species

were found in the open, young and vigorous stages yet only the natives and B. davidii

were present in the mature stage.

Fourteen genera and 12 species were between 5 and 2 m tall (i.e., shrubs and

saplings), natives: Aristotelia fruticosa (1, 0.5%),, Coprosmapropinqua (1, 0.5%), C.

rigida (1, 0.5%), C. arborea (14, 24.71 ± 4.54%), C. unknown (1, 0.5%), K. ericoides

(13, 3.00 ± 0.00 %), Hebe salicifolia (1, 0.5%), and non-indigenous: B. davidii (36, 35.54

± 5.03%), Clematis vitalb (1, 0.5%), R. dealbata (3, mean cover 5.33 ± 4.83 %), Rosa

canina (1, 0.5%), S. fragilis (2, 7.75 ± 7.25 %), S. unknown (1, 0.5%) and Ulex

europaeus (2, 26.25 ±11.25%). Coprosma propinqua, C. arborea, K. erocoides

saplings were present in all four stages. The other species were present in at least three of

the four stages.

Twenty-five % of all species occurred in the 2 - 0.3 m statum. Of the 18 forbs, five

were natives with less than 1% frequency and cover. Two (11%) of the non-indigenous

forbs were found at > 5 plot, Conyza bilbaona (8 , 0.5 ± 0.00 %) and Lotuspedunculatus

(5,1.0 ± 0.50 %). There were no species in the 2 - 0.3 m stratum with cover estimates >

1.33% (Appendix II). No native grasses in 2 - 0.3 m stratum were found more frequently

than at 5% of the plots and yet, fives species of non-indigenous grasses were found at >

5% of the plots; Agrostis capillaries (11, 2.27 ± 1.28 % ), Anthoxanthum odoratum (15,

0.67 ± 0.17%), Dactylis glomerata (8 , 0.81 ± 0.31 %), Holcus lanatus (20, 1.73 ± 0.73

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. %) andSchedonorusphoenix(\l, 3.21 ± 1.37%). Coriaria arborea was second to B.

davidii in being the most frequent (26 plots) shrub in the 2 - 0.3 m stratum (3.21 ± 1.37

%). Six other species were found at > 5 plots; natives; Coprosma propinqua (8 , 1.44 ±

0.46 %), Hebe salicifolia (6, 2.17 ± 0.53 %), K. ericoides (8 , 4.13 ± 2.37 %)and non-

indigenous: R. dealbata (5, 1.00 ± 0.50 %), S.frigilis (6, 1.33 ± 0.53 %), Ulex europaeus

(11, 6.69 ±2.01%).

There were 216 species < 0.3 m however, only B. davidii, L. pedunculatus, C.

arborea and Ranunculus acris cover measured > 5%. About 81% of all the species in the

< 0.3 m stratum occurred at 10 or less plots. The species most frequently found were

non-indigenous pasture grasses (e.g., Holcus lanatus (51, mean 1.6 ± 0.41% cover),

Anthoxanthum odoratum (36, means 2.60 ± 0.95%), Agrostis capillaries (21, means 2.24

± 0.95%)) and forbs (Hypochoeris radicata (51, mean 1.56 ± 0.41% cover). Trifolium

repens (20, mean 0.75 ± 0.17% cover), Lotus suaveolens (19, mean 1 .68 ± 0.29% cover).

Native Dodonaea viscosa and Griselina littoralis seedlings were present in all four

developmental stages. Saplings or trees of these species were not found. The proportion

of woody species increased in the vigorous and mature stages in comparison with the

open and young stages (Fig. 17; Fs=9.83, P<0.0001). This pattern was most significant

in the Porarari and Arnold catchments where the waterways were creeks (F,=5.78,

P=0.0191) and the aimual precipitation relatively high. In addition, mosses and terrestrial

lichens were observed in the <0.3 m stratum. Although present in the open and young

stages the mosses and lichens were non-existent in the other stages.

The concentrations of foliar N and P of B. davidii progressively increased four-fold

from the open stages to the mature stages along the successional gradient (Fig. 18 ; foliar

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. N: F3=8 .77 , P<0.0001 ; foliar P: p3=6.56, P<0.0007). Overall, foliar N was greater on the

west coast (Factor 1, Fi=5.89, P=0.0180) than on the east coast and in the creeks (Factor

2, Fi=l 1.74, P=0.0011) than in the rivers. B. davidii foliar P concentrations were also

greater on the west coast than on the east (Fi=7.73, P=0.0073) and varied with river type

(Fi=25.07,P<0.0001).

Soil properties and chemistrv

Four catchments were located in the west coast which according to Molloy (1998) is

the most distinctive soil landscape regions in New Zealand. The region is characterized

by a narrow coastal fringe backed by high mountains that were extensively glaciated

during the late Quaternary Period. Today the West Coast experiences very high rainfall

(four to six times greater than the east coast catchments) and mild lowland temperatures

(Molloy 1998). The floodplain substrates are predominantly sandstone in origin (with no

measurable silt or clay). In contrast, the east coast catchments are generally comprised of

recent alluvium.

Soil properties and substrate did not vary significantly across the floodplains among

the four-stage developmental chronosequence in contrast with changes among stages and

factors observed in the plant community. The substrate of all of the floodplains was

predominately small cobble (64 -256 mm), pebbles (4-64 mm) and gravel (2-4 mm) with

some boulders (>256 mm). All rocks larger than 4 mm were removed before sampling.

Gravel constituted the largest percentage (48.8 ± 0.02%) of total mass, with cinder next

(27.6 ± 0.01%) and fines the least (23.6 ± 0.02%), of which > 90% was sand and < 2%

was clay (pooled values across all stages). Soil bulk density (g cm'^) was nearly 2 times

greater in river floodplains than in creekbeds (Fi=5.10, P=0.0277), however, soil bulk

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. density did not differ among stages (Fig. 19). Bulk density of the fine fraction of soil

increased by stage (F3=5.16, P=0.0266) even though it was not influenced by

precipitation or river type. Overall average bulk density was 1.62 ± 0.06 g cm'^ and fine

particulate density was 1.20 ± 0.03 g cm'^. Soils from open and young stages held much

less water (F3 =8.15; P<0.0001; field capacity 37.5 ± 3.26% and 34.6 ± 0.98%,

respectively) than in the vigorous and mature stages (field capacity 46.8 ± 2.59%; Fig.

20). Field capacity in the creeks was greater than in rivers (Fi =4.42; P=0.0398).

The organic horizon was absent in the open and young stages and present in the

vigorous stages more often on the west coast than on the east coast. Soil pH declined

among the stages (F 3=3.75 , P=0.0154) and was lowest in the mature stages on the West

Coast than on the East Coast (F,=43.21, P<0.0001). Although a 1.5-fold increase in the

N pools (g m'^) was found between the open and young stages and a 2.3-fold increase

between the young and the vigorous stages,only total N in the open stage soils (3.83 ±

0.64 g m'^) were significantly different from those measured in the other three stages

(P<0.0001; Fig. 21). Soil total N plateaued in the vigorous and mature stages. Total

nitrogen were 2-fold greater on the West Coast than on the East Coast (Factor

1 :Fi=l5.53, P=0.0002) but there was no difference between river types. The relationship

between soil N (g m"^) and above ground B. davidii biomass (g m'^) was positive (Fig 22;

r^ = 0.21911; F 2,?3= 19.92, P<0.0001). Markers indicating developmental stage show a

gradual increase in soil N corresponding with the development stage of the B. davidii

plant community

The mean soil organic C (g m'^) increased six-fold from the open to mature

successional stages with greatest increase occurring between the vigorous and mature

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. stages (Fig 23; F3=8.24, P<0.0001). There was a positive relationship between soil C (g

m"^) and above-ground B. davidii biomass (Fig. 24; r^ = 0.30; F 1,72= 30.01, P<0.0001).

Available P (g m'^) tripled from the open to the vigorous stages before stabilizing (Fig

25; F3=10.24, P<0.0001). Available P on the west coast was about 2-fold greater than on

the east coast (Factor 1: Fi=10.35, P=0.0021). Creek available P was about 1.5-fold

greater than those measured on rivers (Factor 2: Fi=5.04, P=0.0285) Increases in

available P corresponded to above-ground B. davidii biomass (Fig 26; r^ = 0.24; F ,,73 =

22.84, P<0.0001).

Discussion

Consistent with Bellingham and others (2005), Buddleja davidii dominated the open,

young and vigorous developmental stages ( 0 - 8 yrs after flooding) on the exposed

floodplains, elevated channel islands and on the edges of riparian terraces. After this

time, the species declined in frequency and cover. The open stage (i.e., most recently

disturbed by floods) was dominated by even-aged B. davidii seedlings (<10 cm tall).

The seedlings were established on cinder and sand, and in the crevices among the

boulders and cobble (Fig. 5). Buddleja davidii shrubs between 5 - 12 m tall were absent

on four of the floodplains and rare on the other three floodplains (about seven times less

than in the other stages) where they were present only on the edges of riparian terraces.

Shade intolerant, B. davidii of all ages was absent in the interior of riparian forests.

The plant successional trajectory of the B. davidii-Aommaieà community progressed

from flood to native and non-indigenous forbs (e.g., native: Roulia spp., non-indigenous:

Trifolium spp.) and grasses (e.g., native: Cortaderia richardii, non-indigenous: Holcus

lanatus) to woody shrubs and trees (e.g., native: Coriaria spp., non-indigenous: Salix

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. spp.). Buddleja davidii cover was often 20 times greater than that of any other species,

native or non-indigenous. Only twenty-three of the 282 plant species, native and non-

indigenous, contributed more than an average of 3% of the total vegetative cover. The

native riverbed forbs (e.g., Raoulia spp., Epilobium spp.) and grasses {Cortaderia spp.)

characteristic of “natural” New Zealand floodplains (i.e., not invaded by B. davidii;

Cockayne 1927, Gibb 1994, Wardle 1991) were present in low frequencies (< 2%) and

had low cover (< 3%). One native pioneer, C. arborea was present at 20% of plots with

an average cover of 37.5 ± SE 2.73%. C arborea is known to facilitate native as well as

non-indigenous taxa including B. davidii (Bellingham et al. 2001, Walker et al. 2003,

Bellingham et al. 2005).

Buddleja davidii’’s invasion of New Zealand floodplains is comparable to the

phenomenon of woody encroachment that has occurred during past 50 -300 years in parts

of Africa, South American, North America and Australia. Woody species encroachment

coincides with the introduction of non-indigenous species, changes in the disturbance

regimes or both, and has transformed grasslands to forests (MacDonald 1989, Scholtz and

Chown 1993). The changes in ecosystem structure precipitated by woody encroachment

my affect local and regional biodiversity, hydrology and biogeochemical cycling. In the

arid savanna of southern Africa habitat transformation result from the invasion of

Prosopis spp. and have led to the displacement of native grasses and the formation of

large thickets that are impenetrable to livestock (McDonald 1989).

On New Zealand floodplains perennial forbs and grasses are the native pioneer plants

that historically arrived after floods however, these species appear to be the causualities

of the B. davidii invasion. Native pioneer plant species were replaced by B. davidii and

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. therefore, may be driven to (local) extinction. However the presence of B. davidii on the

floodplain may also facilitate the recruitment of native and non-indigenous woody plant

species. Buddleja riav/ri/7-dominated plant communities have greater structural diversity

in comparison with native plant commimities (pers. obs.). Plant commimity structure and

stature have been linked with native species recruitment from perching birds depositing

seeds in their feces (Ferguson and Drake 1999, Shiels and Walker 2003). The presence

of native seedlings of species that have bird dispersed seeds in the B. davidii understory

(e.g., Griselinia littoralis) suggests that B. davidii has a facilitative impact on native

species native recruitment. Increase soil moisture and nutrients in the understory may

facilitate seedling recruitment. Thicket-forming species can facilitate recruitment of later

successional species by additions of organic matter and shade (Walker et al. 2003).

The functional significance of the loss of native pioneers should to be investigated.

In general, the impacts of individual plant species on ecosystems and succession have

been determined to be important (Wardle 2002, Gessner et al. 2004, Zavaleta and Kettley

2006). Species that are infrequent or have little biomass may be considered minor or

subordinate species (Carino and Daehler 2002, Lyons et al. 2005, Boeken and Shachak

2006). The removal of rare and uncommon species has lead to the disruption of

interactions among subordinate and dominant grass and forb species in tall grass prairies

(Smith and Knapp 2003) and invertebrates in intertidal zones (Berlow 1999). Therefore

it is likely that the loss of the native pioneer forbs and grasses on the B. davidii dominated

floodplains will have large impacts on plant community structure or ecosystem properties

despite their low frequency or biomass.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. The successional dynamics of the eight floodplains included in this study were

similar to those described by Williams (1979) and Smale (1990) at Urewera National

Park, North Island, New Zealand. Williams (1979) observed on recently flooded

floodplains that when B. davidii colonized before the native species, the native pioneer

species were less abundant than when B.davidii was absent. Smale (1990) determined

that B. davidii displaced the “pioneer” native woody species, Kunzea ericoides and

Leptospermum scoparium. Buddleja davidii most likely accelerated succession on the

fresh alluvium by replacing long-lived native forest species (Smale 1990). Kunzea

ericoides seedlings, saplings, shrubs and trees were present in all four stages on the

floodplain that I surveyed, albeit infrequently and in extremely low numbers.

Leptospermum scoparium was present however, less frequently than K. ericoides. These

results suggests that B. davidii may have altered the typical order of plant recruitment on

these eight floodplains.

However, I must use caution in my interpretation because I deliberately sought

patches on the floodplain of vegetation that were dominated by different age classes of B.

davidii and therefore should reinvestigate whether K. ericoides abundance was greater in

the riparian uplands or on channel islands where B. davidii is usually absent. The

seedlings of several plant species identified by Smale (1990) as being “late successional”

(e.g., Coprosma spp, Pseudopanax spp.) were found in all stages. Whether 5. davidii

inhibits or facilitates their growth would be interesting to determine.

Buddleja davidii foliar N and P concentration increased as the plant community

developed over time. The increase in foliar nutrients suggests that B. davidii was an

efficient forager of N and P in these floodplains. Buddleja davidii assimilates nitrate in

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. its leaves rather than roots or stems and increases the efficiency by which it utilizes

photosynthetic N. Leaf nitrate assimilation is common in ruderal species (i.e, species that

occupy disturbed sites where nitrification rates are generally high; Lambers et al. 2006).

How much of the N, P or both remain in the leaves prior to abscission has not been

determined. However, Matson (1990) found that leaves of the Buddleja cogener

increased soil fertility in Hawaii suggesting that B. davidii may have the same impact on

the floodplain soils. Nutrient recycling from litter may not be an issue because there was

virtually no litter accumulation or organic soil development (M. Thomas pers. com, pers.

obs.) in the open and young stages and little in the vigorous and mature stages.

The novel impact that B. davidii had on soil fertility on the floodplain of the Kowhai

River (Bellingham et al. 2005) was evident in this study. The concentrations of N and P

in the soil of several of the floodplains increased commensurate with the stage that the B.

davidii community had developed (Figs. 21 and 25). However, an increase in N and P in

mineral soils is to be expected when vegetative biomass and soil microbial activity

increase. Floodplain soils are extremely low fertily environments as indicated by N

concentrations in the open stage that were 10-times less than those measured in the mature

stage and P levels in the open stage that were 4-times less than those measured in the

mature stage. Buddleja davidiV?, biannual leaf loss may enrich soil fertility. Litter

decomposition on this depauperate substrate can only increase soil fertility in the early

stages even if B. davidii proves to be an effieient remobilizer. Nevertheless, as B. davidii

biomass declines with stand age, other species replace it in the plant community,

contributing to the litter and root exudates that enrich the soil. However greater levels of

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. available P in B. davidii-dommdXeà stands in seven different watersheds strongly suggests

that B. davidii has a role in enriching floodplain soils.

While the characteristics of the specific floodplain may influence the localized

patterns of B. davidii stand development, river and catchment characteristics may

confound the processes. It was not surprising that location and therefore, precipitation

and the type of river heavily influenced the plant community and ecosystem-function.

What did not contribute though was the influence of humans (e.g., land use). The

catchment scale analysis of factors common to rivers infested by B. davidii that I did for

this study was a first attempt at discerning the influence that the landscape may have on

the receptivity of floodplains to invasion by B. davidii. The scale of several of the

landscape attributes may have been too coarse to provide information at the river-scale

(e.g., dominant catchment land use, human density index derived from the number of

dwellings in the catchment) and therefore would not be expected to contribute

significantly to the model as designed.

The presence of naturalized non-indigenous species in New Zealand floodplains is

highly correlated with nearness of the floodplain to landscapes modified by humans

(Timmons and Williams 1991, Williams and Wiser 2005). River beds may be the richest

habitat for naturalized plants excluding urban wastelands (Campbell 1986). Clouds of

wind-blown sand are features of braided floodplains. Deposited sand and silt provide an

abundance of suitable habitat for seed germination (Gibb 1994). The non-indigenous

pioneers identified in this study were primarily pasture grasses and forbs that had been

deliberately introduced to augment soil fertility or as sheep or cattle feed. Over the past

150 years more than 2000 plants have been introduced to New Zealand through the

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. agriculture and horticulture industries (Wardle 1991). Widespread alterations to

floodplain ecosystems that commonly stem from the presence of humans (e.g., grazing,

logging, mining, agriculture, road construction, and hydrologie diversions or alternation)

contribute to an increase in invasive plant species on floodplains (Magee et al. 2007).

Greater exploration of landscape attributes and further analyses are in order before

making assumptions about the relationship between B. davidii and anthropongenic

stressors.

In summary, although there was a great deal of variability among floodplains, the

development of the floodplain plant communities dominated by B. davidii on the South

Island was consistent with those described by Williams (1979), Smale (1990), Wardle

(1991),and Gibb (1997) and Bellingham and others (2005). Despite B. davidii

dominance there were native shrubs and trees present in all four stages as seedlings,

saplings and adults, albeit they were present in low frequencies and had little eover.

There were sequential increases in B. davidii foliar N and P concentrations along the

developmental gradient that stabilized in later stages that suggests that B. davidii

efficiently scavenges nutrients. Soil P and N concentrations also increased

commensurate with an increase in B. davidii biomass. This suggests that B. davidii may

augment soil fertility. Whether B. davidii negatively impacts native vegetation through

competitive inhibition, facilitates native species recruitment or has no fleet are as yet

unclear. I address these three possibilities in Chapters 4 and 5.

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davidii floodplain plant communities.

Canonical Canonical Multivariate F dfi dfi P

Dimension Corr.

1 0.96 5T82 9 166 <0.0001

2 0.73 17.07 4 138 <0.0001

Table 3-3. Standardized discriminant coefficients of attributes used to classify

developmental stages of Buddleja davidii floodplain plant communities.

Canonical Dimension 1 Canonical Dimension 2

Light transmission (%) 0.79 0.28

Buddleja davidii biomass -0.24 -0.64

Buddleja davidii age -0.29 0.61

101

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Raoulia australis Coriaria arborea Griselinia littoralis

Time Figure 8 . Examples of native New Zealand forbs, grasses, shrubs and trees that may establish on floodplains following flooding. The species designated as (a) and (b) generally appear first. However, the order and timing of the establishment of species designated as (c) through (f) are variable and may occur in series or simultaneously..

103

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o m

105

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. open Upland vegetation f young 3opan 3 young 4 vigofous vigorous 2 mature mature

«fcimiviartecl plant commurirty

' Uptand vegetation [Floodplain | Gravel road B 3% 3m»pk* Pasture

Putil Putil River

Upland vegetation young 4 open 4 young 3 vigorous im a tu ie

Succttssionol daoBS RuMkyo tiaininadod plamoanHrainly ^ Upland vegetation ^

B 3x3m»plal

Gravel road

Oaro River Figure 11. Schematic of Buddleja davidii-sarvey design. Several 3 x 3 m plots were established in Buddleja davidii-àormnaieà plant communities selected to represent a four- stage developmental (i.e., open, young, vigorous and mature) chronosequence (i.e., time since disturbance by flooding; Fig. 10) on the Puhi Puhi River and Oaro River floodplains.

106

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2P .2I I .n B -o I I m > u X '8 1Cw m T3 O .rf, R ~r T I T, n n rf, ê 8 B .1 I I

107

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. I)E\TLOPMKNTAL STAGE OPEN YOUNG * VIGOROUS MATURE

6E 100 70

-4 5 6 ■ S Buddleja age (yis)

Figure 13. Relationship between log transformed Buddleja davidii biomass (y: log scale) and Buddleja davidii age (jc) of 3 x 3 m plots, The regression: y = 2.09 (x) + 0.45 x (x) (r^ = 0.31, P < 0.0001, n = 71). Data points corresponding to each Buddleja davidii developmental stages are shown in the legend.

108

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. (a) (b)

: Conway * M6Whinui Waiho

Hapuku * CN I (c) cd Ph ’(d )'

— 1 O m ihi* Porarari Arnold

-2

- 2 -1 0 1 Factor 1

Figure 14. All catchments plotted with respect to the first and second factors. Factor 1 separated catchments based upon which coast they were located; (a) = west coast and (b) = east coast. Factor 2 separated catchments based upon river type (c) river and (d) creek.

109

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 2 0 -

10 -

West East Coast

Figure 15. The plant species richness of 3 x 3 m plots designed to represent a four-stage chronosequence of Buddleja c/av/Jü-dominated plant communities ( y ) plotted by coast (jc) (South Island, New Zealand). When error bars (95% confidence limits of the mean) overlap there was no statistical difference between the coasts.

110

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 100 (a) west coast least coast 90

SO ( b ) y r 1 70

6lj -S 5 0 \ (b) 4 0 T 30 1 1 20 1 S OQ > œ g o ? S 5 é < o S < æ X 2 <î5 (X

C a tc h m e n t

Figure 16. Percentage of non-indigenous species per 3 x 3 m plots designed to represent a four-stage chronosequence of Buddleja cfafv/V///-dominated plant communities (y) plotted by seven South Island, New Zealand catchments (jc) . The (a) labels denote on which coast the catchments are located and the (b) labels denote which waterways were creeks. When error bars (95% confidence limits of the mean) overlap there was no statistical difference between catchments.

I l l

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 0.60

a O' 0.45- 4> 0.40- § ^0.35-

p 0.30-

0.25-

0 , 20 -

0.15 OPENYOUNG

Developmental Stage

Figure 17. Percentage of woody plant species (y) in 3 x 3 m plots that represent a four- stage chronosequence (jc: open through vaàXür€)oiBuddleja davidii-àommaXQà plant communities on floodplains on the South Island, New Zealand. When the error bars (95% confidence limits of the mean) overlap there was no statistical difference between means of the developmental stages.

112

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. o c

0.35

0,30-

0,25-

0 , 20 -

0,15 OPEN YOUNGMATURE

Figure 18. Buddleja davidii foliar N (%) and P (%) concentrations (y) from plants in 3 x 3 m plots that represent a four-stage chronosequence (x-axis: open through mature) on Buddleja davidii-àoramaXQà floodplains on the South Island, New Zealand. When the error bars (95% confidence limits of the mean) overlap there was no statistical difference between means of the developmental stages.

113

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. s 1. 6 -

CREEK RIVER

RIVER TYPE

Figure 19. Soil bulk density (g cm'^; y) of soils from 3 x 3 m plots that represent a four- stage chronosequence 'mBuddleja davidii dominated plant communities plotted by river type (x). When error bars (95% confidence limits of the mean) overlap there was no statistical difference between means of the river types.

114

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 50-

35-

CREEK RIVER

FIVER TYPE Figure 20. Soil field capacity (%; y) of soils from 3 x 3 m plots that represent a four-stage chronosequence in Buddleja davidii dominated plant communities plotted by river type (x). When the error bars (95% confidence limits of the mean) overlap there was not no statistical difference between means of river type.

115

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 25

:o-

,^ 1 5 2

% ~p CO 10-

OPÈN YOUNG VIGOROUS XL4TURE

D EVELO PM EN TAL STAGE Figure 21. Soil total nitrogen (g m'^; y) of soils from 3 x 3 m plots that represent a four- stage chronosequence in Buddleja davidii dominated plant communities plotted by developmental stage. When the error bars (95% confidence limits of the mean) overlap there was no statistical difference between means of the developmental stage.

116

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. DEVELOPMENTAL STAGE______. OPEN ^ YOUNG » VIGOROUS n MATURE

log Biiddlejii biomass (g nv -2) Figure 22. Relationship between soil total nitrogen (g m" ; y Box - Cox transformation) and log Buddleja davidii biomass (g m'^; x log transformed) in 3 x 3 m plots from Buddleja davidiz-dominated floodplains on the South Island, New Zealand. The legend indicates the development stage. The regression: y -■ 2.83 + 1.20 x(jc)(r^ = 0.22, P < 0.0001, n = 73).

117

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 0.020

0.015-

R 0.010-

^ 0.005-

0.000 OPENYOUNG VIGOROUS M4TURE

DEVELOPMENTAL STAGE

Figure 23. Soil organic carbon (g m'^) of soils from 3 x 3 m plots that represent a four- stage chronosequence in Buddleja davidii dominated plant communities plotted plotted by developmental stage (x). When the error bars (95% confidence limits of the mean) overlap there was no statistical difference between means.

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. -0.003 DEVTLOPMENT.AL STAGE • OPEN -0 004 ♦ YOUl'IG X VIGOROUS a -0.005 (I MATURE

g -0 006 C3 y. -0.007

X -0.008 m V -0 009 S B -0 01 o ^5 -0 011

-0 .0 1;

-0.013 -1 2 3 4 5 Buddleja biomass (g nv -2 ) Figure 24. Relationship between soil organic carbon (g m' ; y Box - Cox transformation) and log Buddleja davidii biomass (g m' ; x log transformed) in 3 x 3 m plots from Buddleja (/ovidn'-dominated floodplains on the South Island, New Zealand. The legend indicates the development stage of each sample. The regression; y = -0.01 + .00065 x (x) (r^ = 0.30, P < 0.0001, n = 73). The markers corresponding to each Buddleja davidii developmental stages are shown in the legend.

119

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 0.14

0 . 10 -

r I I 0.08- 3 3 Ph 0.06- o CO

0 04-

0 . 02 -

000 OPEN YOUNG VIGOROUSMATURE

DEVELOPMENTAL STAGE Figure 25. Soil available phosphorous (y: g m" ) of- 2 soils\ from 3 x 3 m plots that represent a four-stage chronosequence in Buddleja davidii dominated plant communities plotted by developmental stage. When error bars (95% confidence limits of the mean) overlap there was no statistical difference between means of the developmental stages.

120

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. . OPEN » YOUNG X VIGOROUS -0,05- q MATURE K m

0 1 4 6 8 loe Biiddleia biomass ( 2 m Figure 26. Relationship between soil available phosphorous (g m" ;y Box - Cox transformation) and log Buddleja davidii biomass (g m'^; x log transformed) in 3 x 3 m plots of Buddleja ifov/jü-dominated floodplains on the South Island, New Zealand. The legend indicates the development stage of each sample. The regression: ); = -0.13 + 0.007 X (%) (r^ = 0.24, P < 0.0001, n = 73). The markers corresponding to each Buddleja davidii developmental stages are shown in the legend.

121

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 4

THE INFLUENCE OF AN INVASIVE SHRUB,

BUDDLEJA DAVIDII, ON A NATIVE SHRUB,

GRISELINIA LITTORALIS, TRANSPLANTED

INTO A NEW ZEALAND FLOODPLAIN

CHRONOSEQUENCE

Abstract

The long term impacts of Buddleja davidii, an invasive shrub of native to China, on

plant community development in New Zealand floodplains are not known. Buddleja

davidii may inhibit the establishment of native species on New Zealand floodplains and

therefore, may alter successional trajectories. Griselinia littoralis, a native New Zealand

shrub, was planted in plant communities dominated by B. davidii in three New Zealand

floodplains to determine to what extent B. davidii may facilitate or competitively inhibit

the establishment of a native species. The G. littoralis plants (600) were transplanted in

B. davidii-àommaiQà plant communities that represented a three-stage developmental

(i.e., open, young, and vigorous) chronosequence (time since last flood) for two growing

seasons. The means of the above- and below-biomass, height, specific leaf area and root

to shoot biomass ratio were compared by developmental stage, river and both using

analysis of variance. Above-ground biomass, height and specific leaf area of the G.

littoralis plants remained unchanged from when initially planted in the open and young

122

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. developmental stages yet the G. littoralis plants in the vigorous stages had nearly doubled

in height and specific leaf area. The increase in G. littoralis height and specific leaf area

under the closed B. davidii canopy suggests that B. davidii may have enhanced the

growth of the G. littoralis transplants. Soil moisture and nutrients were greater under the

B. davidii canopy in the vigorous stages than in the open or young stages (i.e., four-fold

increase in soil nitrogen and two-fold increase in phosphorus in the vigorous stages in

comparison with the open stages). Stem density in the B. davidii vigorous stage was

greater than in the open or young stages which may have protected G. littoralis plants

from herbivory by introduced herbivores (i.e.. Ova aries [feral sheep], Oryctolagus

cuniculus [rabbits] and Lepus europaeus [hares]). Griselinia littoralis seedlings

established naturally beneath the B. davidii canopy, yet were not established in the open

or young stages suggests that B. davidii does not inhibit G. littoralis establishment The

low light characteristic of the vigorous stage may eventually inhibit B. davidii and

facilitate native plant species recruitment.

Introduction

Plant species that establish in early succession can facilitate recruitment of the plant

species that generally establish later in succession. Early successional plant species can

also inhibit the colonization by subsequent species by using available resources more

efficiently than the other species (Connell and Slatyer 1977, Walker and Chapin 1987). .

In the first scenario early successional species that colonize after a disturbance may

modify the environment such that the environment becomes less suitable for subsequent

intra-specific recruitment but may become more suitable for the recruitment of late

123

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. succession species (i.e., facilitation model). For example, plants that colonize after

flooding disturbance on a floodplain are generally opportunists that can readily establish

and reproduce on the recently exposed substrate. The growth and reproduction of the

initial eolonists well be suppressed as light levels are reduced by the coalescing canopy.

Eventually, the shade-intolerant pioneer speeies will not beable to survive. However the

conditions will become suitable for late successional plant species that are shade-tolerant.

In the second scenario, the earliest colonizers may modify the environment in ways that

will inhibit inter- and intra-specific recruitment.

Native plant species have evolved adapations that enable them to tolerate the

conditions of the native plant community. The successional stages that typically develop

after disturbance on floodplains in temperate regions (i.e., open to herbaceous dicots to

woody shrubs to trees) are evident in New Zealand systems however, the native speeies

prevalent within one stage are not necessarily replaced in another stage; rather the

dominance among species may shift over time (Dansereau 1964; Wilson 1990).

Non-indigenous plant species that colonize denuded landscapes generally share the

same eharacteristics of native pioneer species. They arrive early, establish quickly and

use resources efficiently (Thompson et al. 1995). Early arrival may be the crucial factor

in determining whether one species, native and non-indigenous, will out-compete

another. A survey of 79 independent studies of plant performanee (e.g., growth rate,

photosynthesis, germination, survival) between native and invasive plants in all the major

geographic regions of the world revealed that native species were superior performers in

94% of the studies (Daehler 2003). However, in environments associated with human

activities the plant invaders consistently had a competitive advantage over native plant

124

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. species (e.g., increased growth and photosynthetic rates, greater percentage of germinates

and survival; Daehler 2003).

The general pattern of floodplain succession in New Zealand, regardless of species

nativity, is that early forbs (e.g., native; Raoulia spp., Epilobium spp., non-indigenous:

Trifolium spp.) establish on the exposed surfaces. Grasses (e.g., native: Cortaderia spp.,

non-indigenous: Bromus spp.) soon follow; however they are often co-dominant with the

forbs. Eventually the community will transition from understory forbs and grasses to

woody shrubs (e.g., native: Coriaria arborea, non-indigenous: B. davidii) and trees (e.g.,

native: Kunzea ericoides, non-indigenous: Salix fragilis) that will dominate until the next

flood or other disturbance resets the process (Wardle 1991; Bellingham et al. 2005;

Williams and Wiser 2004). The substitution of an invasive for a native species at any

time during the cycle may delay or deter (i.e., inhibition) or accelerate (i.e., facilitation)

the entry of a native species. However, the consequences of an invasive species replacing

a native species at any time during the cycle are unknown.

The perception that all biological interactions among invasive and native species are

negative is based upon a few seminal studies (i.e., the N fixer in Myrica faya in Hawaii

(Vitousek and Walker 1989), or the rapidly transpiring, Tamarix ramosissima in the

southwestern USA (Sala et al. 1996)). Yet there is evidence that invasive plants can

facilitate the recruitment of native species by providing shade and mechanical protection

against ungulates in secondary shrublands in mountane Argentina (Tecco et al. 2006).

Buddleja davidii Franchet, a woody invasive native to China, that has naturalized on

New Zealand floodplains. Buddleja davidii dominates in the early stages of plant

succession on some New Zealand floodplains (Chapter 3). After New Zealand forest

125

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. plants are generally tolerant of a wide range of ecological conditions (Dansereau 1964).

Native species (e.g., Griselinia littoralis) that are equally able to germinant and establish

in the open light as well as dense shade may be able to tolerate the low light levels that

develop as non-indigenous woody shrubs and trees mature on the floodplain.

This study examines the interactions between an invasive pioneer, B. davidii and a

native shrub, Griselinia littoralis Rauol Choix on three New Zealand floodplains to

determine whether the biological interaction between the two species facilitates or

competitively inhibits the establishment of the native species when the invasive species is

already established. Griselinia littoralis saplings were transplanted into B. davidii-

dominated plant eommunities selected to represent a three-stage developmental

chronosequence of time since disturbance by last flood (i.e., open, young and vigorous).

I hypothesized that B. davidii would impact the growth of G. littoralis transplanted in a

chronosequence of 5. c/av/c/n-dominated stands. However, impact whether it be the

positive (e.g., facilitative), negative (e.g., competitive inhibition) or both will vary based

upon the developmental stage.

Methods and Statistical Analysis

Griselinia littoralis cuttings were transplanted in B. davidii-dominated stands on the

floodplains of three New Zealand east coast rivers (Fig 27): Puhi Puhi River (easting

2570812, northing 5881131; NZ Map Grid), Kowhai River (easting 2555965, northing

5874623; NZ Map Grid) and Conway River (easting 2546423, northing 5844111; NZ

Map Grid). The Puhi Puhi and Conway rivers were selected because three of the four

developmental stages of 5. davidii as described in Chapter 3 (Fig. 27) were present on the

126

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. floodplain. The survey of floodplains invaded by Buddleja davidii determined that there

were fewer mature (i.e., > 10 yr) B. davidii plant communities on floodplains than plant

communites in the open, young and vigorous developmental stages therefore the mature

developmental stage was not included in this study. Buddleja davidii-éomm&Xcà plant

communities on the Kowhai River were examined by Bellingham and colleagues (2005).

Methods to establish plots are described in Chapter 3 and Appendix VI. The total

number of plots selected in each floodplain depended on field logistics and the abundance

and distribution of B. davidii present.

Fourty B. <7av/c/ü-dominated stands were selected to represent the three

developmental stages chronosequence (Puhi Puhi River; 4, 7, 4; Kowhai River: 4, 6, 5;

Conway: 4, 4,2 in the open, young and vigorous stages, respectively). Methods how

plots were established and stages characterized are described in Appendix VI.

Griselinia littoralis plants were cultivated from South Island cuttings and grown in

potting mix at Southern Woods Nursery in Christchurch, NZ. After being delivered from

the nursery, the 30-cm tall plants were allowed four weeks to transition from the nursery

to shade houses then placed outside in the shade for five days before being transplanted

in the river plots, during this time they were watered as necessary. At each plot, 15 G.

littoralis transplants were planted into 10 cm deep holes per plot (Fig. 28; aligned in a

grid of four rows of four, each space was approximately 20 cm apart; one space

(randomly determined) was left empty per plot; Figs. 28). The river and plot that each

plant was actually placed was determined randomly. Initial height was measured

immediately after planting. Mortality and condition (i.e., vigor, leaf color, animal

browsing and damage) were recorded after 24 weeks. Immediately before the plants were

127

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. transplanted, plot-level plant community, B. davidii foliar chemistry and soil properties

and chemistry measurements were collected as described in Chapter 3.

In February 2007, after two growing seasons in the field (76 wks), surviving

transplants from all undisturbed plots were harvested (Fig. 29). Plant height was

recorded prior to removing from the ground. An estimate of plant growth was

determined from A height = final height - initial height (henceforth referred to as

growth). Leaves, stems and roots of each transplant were separated. Total leaf area was

calculated on fresh leaves from each transplant using a scanner and WinFOLAR

computer image analysis software (Regent Instruments, Inc., Quebec City, Quebec,

Canada). Specific leaf area (SLA; i.e., a measure of leaf density and thickness) was

determined by dividing total leaf area by total dry leaf mass. Leaves, stems and root were

dried at 35”C for 5 days before determining dry mass of all leaves and stems; root dry

mass was determined onl on three randomly selected plants per plot.

Statistical Analvsis

A direct discriminant function analysis was performed using three plot-level variables

as predictors that data could be grouped by successional stage as described in Chapter 3.

Predictors were B. davidii age (i.e., number of tree rings), percent light transmission of

the total ambient and total B. davidii biomass. Groups were successional stages of

development (open, young and vigorous: SAS Institute Inc., Cary, NC, USA; Tabachnick

and Fidell, 1996).

To determine the effects of stage and river on G. littoralis transplants, G. littoralis

shoot and root biomass, root: shoot biomas ratio, specific leaf area (SLA) and growth

were compared between successional stages and rivers using individual analyses of

128

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. variance (PROC GLM) with Tukey a posteriori tests on the differences among least

square means among rivers and stages and interactions as applicable (SAS 9.1, SAS

Institute Inc., Cary, NC, USA). Test-wise probabilities were calculated using Bonferroni

corrections. When growth was less than at the start, which did occur when transplants

were heavily browsed and/or they settled slightly into the ground after planting, the

growth or change in height was set to equal zero. Analyses of the residuals were used to

determine whether data met assumptions (i.e., normality, equal variances and scaling).

Data were transformed (root weight - l)/0.03 for G. littoralis root biomass, log for

specific leaf area and log for growth) as needed to meet data assumption (i.e., normality,

equal variances and scaling). Outlier observations (f<0.05) and influential observations

(i.e., cases where the scaled measure of the change in the predieted value of that

observation was > 2, referred to as the Dffits statistic) were removed if transformation did

not correct effects. Residuals were plotted to confirm correction. All statistical analyses

in this study were performed using SAS 9.1 (SAS Institute Inc., Cary, NC, USA).

Results

Successional stage classification

Tests of dimensionality for the discriminant analysis, as shown in Table 4-1, indicate

that both the dimensions are statistically significant. Dimension 1 had a canonical

correlation between the response variables and the stage of development of 0.94, whereas

the second canonical correlation dimension was lower (0.54). Table 4-2 presents the

standardized canonical coefficients for both dimensions.

129

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. The first discriminant dimension is positively weighted by B. davidii biomass (0.51)

and B. davidii age (-0.54) and strongly negative on light (0.77; Fig. 30). The second

discriminant dimension is slightly dominated by light. These results indicate that the first

dimension reflects a bipolar B. davidii biomass and age dimension while the second is a

light dimension. As shown in Fig. 30, the first canonical dimension maximally separates

the open and young (left clusters) from the vigorous (right cluster) stages. The second

canonical dimension discriminates the open from the young. Based upon these analyses

the a prioir classification of the sample plots was accepted for further analysis.

Griselinia littoralis Transplants

Two hundred and five transplants (34.2% of the total) were lost because of floodplain

excavation (15%) in the Kowhai and flooding (5%) and browsing by feral sheep (Gvo

aries), rabbits {Oryctolagus cuniculus) and hares {Lepus europaeus', 85 [14.2%]) in the

Puhi Puhi River. Of the 110 surviving transplants at the Puhi Puhi River, only 4%

showed an increase in shoot biomass or height beeause of heavy damage from browsing.

Therefore, the Puhi Puhi River was removed from the analysis of variance, leaving 19

plots (285 transplants; 47.5 %) remaining. There was 100% survival of transplants in the

plots that were not damaged by excavation or flooding in the Kowhai and Conway

Rivers.

The shaded conditions in the vigorous stage of succession had a significant effect on

the shoot and root biomass, root to shoot biomass ratio, specific leaf area and growth of

the G. littoralis transplants (Table 4-3). Griselinia littoralis shoot biomass was slightly

greater at the Kowhai (10.6 g ± 0.29) than at the Conway River (9.1 ± 0.25 g; Table 4-3;

Fig. 31).

130

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. There was a nominal stage effect as well (Table 4-3) however the mean shoot

biomass in the vigorous plots at the Kowhai River was almost two-fold greater than at

any of the other stages at either the Kowhai or Conway Rivers (i.e., explaining the

significant river x stage interaction). Growth and specific leaf area of G. littoralis in the

Conway and Kowhai Rivers remained unchanged from when initially planted in the open

and young plots yet was nearly doubled in the vigorous stage (Fig. 32., F2,i=13.74,

P=0.0002; Fig. 33; Fz,,=36.26, P<0.0001).

The developmental stage of 5. davidii in both rivers influenced the below-ground

biomass. In the vigorous stage, G. littoralis root biomass decreased (F 2,2 = 9.33,

P<0.0004; Table 4-3; Fig. 34) and therefore, the G. littoralis root to shoot biomass ratio

was much greater in the vigorous stages then in the open or young stage (F 2,2 = 19.86,

P<0.0001; Table 4-3; Fig. 35). Root biomass was greater in the Kowhai than in the

Conway River (Fi ,2 - 4.75, P<0.0340; Table 4-3; Fig. 36).

Discussion

The dense B. davidii canopy, as found in the vigorous stage, was important to G.

littoralis transplants in all three rivers. The increase in G. littoralis height in the vigorous

stands in comparison with the unchanged conditions of the above-ground growth of G.

littoralis in the open and young stands can be attributed to the understory habitat beneath

the B. davidii canopy. Thicket-forming species can facilitate later successional species

by additions of organic matter and shade (Walker et al. 2003). Griselinia littoralis

seedlings were established naturally in the B. davidii understory yet were not established

in the open or young stages provides additional evidence that B. davidii does not inhibit

131

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. establishment by G. littoralis. Conversely, Wilson and others (2004a) found that B.

davidii seeds do not germinate in the dark. I did not find any B. davidii seedling in the

understory of the B. davidii canopy in the vigorous stage. Buddleja davidii relative shoot

growth rate was dramatically reduced and mortality was significantly greater under light

levels found in mature New Zealand forest (Chapter 5) in comparison with cuttings

grown in light levels comparable to those measured in open and young stands (90% and

27%, respectively). Even though the low-light levels in the understory of the vigorous B.

davidii stands are unsuitable for B. davidii recruitment, B. davidii stands may be

facilitating the eventual replacement by G. littoralis or other co-dominant native species.

Established in patches of shrubs (bush) in forest, grasslands and floodplains at low-

and mid-elevations, G. littoralis is highly adapted to tolerate a range of light, moisture

and temperature regimes (Dansereau 1963, Wardle 1991). Seedlings will establish on

trees, mossy boulders or logs, or on the ground where the undergrowth is sparse (Wardle

1991). Like most New Zealand native trees, G. littoralis has a high degree of shade

tolerance (Pook 1979, Wardle 1991, Standish et al. 2001, Walker et al. 2003) and can

establish as a pioneer or as a later successional invasive (Wardle, 1991, Walker et al.

2003). Several factors such as increased moisture and soil nutrients and protection from

herbivores may have facilitated survival and growth of the G. littoralis transplants under

the B. davidii canopy.

Canopy closure changes the amount of radiant energy available to the understory, soil

temperamre and evaporation. The light levels in the closed canopy were much lower in

comparison to the open and young stages. The leaves on the G. littoralis transplants

exposed to the sun had damage thatwas attributed to sun damage (i.e., brown and black

132

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. spots) that were not present on the transplants beneath the B. davidii canopy. The B.

davidii canopy also reduced loss of moisture. Field capacity measurements (Appendix

VI; i.e., amount of soil moisture held in the soil after excess water has drained away)

indicated that soil moisture was approximately 1.5-fold greater in the vigorous plots in

the Kowhai River than in the open or young plots (Appendix VI). In addition, the soils

and foliage appeared beneath the B. davidii eanopy in comparison to the conditions

beneath the young and open stages in both rivers (pers. obs.). Because,water relations are

often important to seedling survival, especially for native tree species in New Zealand

(Wardle 1991, Foutain and Outred 1991, Rowarth et al. 2007) the moist conditions in the

understory may facilitate the germination of G. littoralis seed dropped by birds in their

feces. Research on the relative importance of the microsite environment of the B. davidii

understory to G. littoralis and other native species is needed.

Buddleja davidii stands that were vigorous and mature (this study and Chapter 3;

Appendix VIII) had dramatically higher soil fertility compared with the earlier stages,

suggesting indirect facilitation of succession from soil development. The positive

relationship between G. littoralis and B. davidii biomass was similar to the relationship

found between G. littoralis and Coriaria arborea (a pioneer native, N-fixing shrub;

Walker et al. 2003). Walker et al. (2003) found that G. littoralis establishment was

promoted by increased soil fertility. Perhaps G. littoralis’’s growth was enhanced by the

enriched soils beneath the vigorous B. davidii stands. Griselinia littoralis is strongly

mycotrophic and has been reported as weakly responsive to added phosphorus (?)

because the mycorrhizal system of G. littoralis is adapted to generally low concentrations

133

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. of available P in native soils (Baylis 1959, Wardle 1991). Yet, Bellingham et al. (2001)

also found that G. littoralis responded positively to inputs of N-rich litter.

The increase in soil fertility in this study verifies the results of the B. davidii

survey of seven New Zealand catchments (Chapter 3). The B. davidii survey included

stands representing four stages of B. davidii development: open, young, vigorous and

mature. The relationship between B. davidii biomass and soil N and P was complicated

by an initial increase followed by a decrease in nutrients as B. davidii biomass increased.

When the data from the mature stands were removed, the relationships were similar to

that of the transplant study. The dramatic increases in concentrations of foliar N and P in

B. davidii (this study and Chapter 3) suggest that B. davidii nutrient uptake increases over

time as well. Although not measured during this study N and P concentrations in the

litter beneath the B. davidii canopy, may be major contributors to soil fertility. The litter

of B. asiatica is N-rich and decomposes easily compared with native litter in primary

succession forests in Hawaii, leading to increased soil nutrients beneath the canopy of

the invasives (Matson 1990). Further research may find that the litter that accumulates in

the B. Jav/Jü-dominated stands may be an important source of N and P for recruitment

for both native and non-indigenous species (Bellingham et al. 2005).

In addition to the conditions in the B. davidii understory facilitating G. littoralis, the

thicket-forming B. davidii may have also physically prevented the transplants from being

browsed. G. littoralis is susceptible to browsing because of its palatable leaves that are

soft, glabrous and high in nutrients (Wardle 1991). At the Puhi Puhi River, feral sheep,

rabbits and hares browsed on the G. littoralis transplants even though the floodplain plant

community was rich in palatable native and non-indigenous plants. Only in the vigorous

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. stands were the transplants not browsed suggesting that woody cover may have protected

them from being eaten or damaged (Huntly 1991). However, this is contrary to typical

hare behavior because hares do not burrow; instead they live in forms or shallow scrapes

in the soil above ground amid dense sheltering vegetation (Hoffmann and Smith 2005).

The dense vegetation of the vigorous thickets would have been ideal habitat for hares.

The browsing patterns of three different herbivores were noticeably different. Sheep

ate the tops of the transplants, leaving the leaves and stems to resprout. Regrowth on

transplants that had only the tops removed accounted for all the regrowth on surviving

plants at the Puhi Puhi River. The sheep also removed the transplants, leaving them near

the plots with the tops removed. The hares and rabbits removed the leaves and ate

through the base of the stems, killing the plants rather than promoting regrowth.

There was much evidence of the presence of all three herbivores (i.e., scat and tracks)

found at all three rivers, yet only at the Puhi Puhi River were the transplants browsed.

The degree of damage inflicted upon a plant community by herbivores, although often

driven by the availability of preferred food (Parsons et al. 1994, Bowen and van Vuren

1996, Doland et al. 2002) is extremely complex and beyond the scope of this study.

Nevertheless, these results are noteworthy because the browsers preferred the native G.

littoralis over other forbs and grasses established on the riparian edge of the river (e.g.,

non-indigenous: Lotuspedunculatus, Trifolium spp.). Grazing preference for G. littoralis

in the Puhi Puhi River yet not in the Conway or Kowhai Rivers suggests that there may

be selection for native seedlings in some floodplains but not on others. Herbivores can

dramatically alter plant form (Huntly 1991) as was seen in the increased root biomass of

G. littoralis transplants that had been browsed on the Puhi Puhi River. Future research

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. should address what influence, if any, the preference of native plants species over non-

indigeneous species by herbivores has on succession in some rivers and identify

relationships between floodplains and herbivore preferences.

Natural G. littoralis seedlings in the understory support my suggestion that B. davidii

facilitates recruitment. Forest succession is dependent upon the arrival of propagules of

species tolerant of the evolving environment (McClanahan 1986, Duncan and Chapman

1999). The arrival of the seeds can be facilitated by birds (Shiels and Walker 2003).

However, vegetation structure strongly influences the perching behavior of frugivorous

birds and so may impact the deposition patterns of bird-dispersed seeds (Ferguson and

Drake 1999, Shiels and Walker 2003). Seedling recruitment of native canopy species in

New Zealand is largely dependent on bird-dispersed seed rain (Williams 1983, Wardle

1991, Rowarth et al. 2007). Vigorous stands of B. davidii are characterized by many

multi-stemmed shrubs, between 2 -5 m tall, with rigid stems. Whereas the vegetation in

the open and young stands was often less than 2 m tall and pliable it did not provide suit

perches for birds. The presence of bird droppings and native G. littoralis seedlings in the

understory of the vigorous B. davidii stands suggests that B. davidii facilitate seed

dispersal by serving as perches.

Ultimately, the transition of the floodplain plant community from predominantly B.

davidii to a mosaic of native species will be driven by the ability of the native seedlings

to tolerate the habitats created by B. davidii. In summary, G. littoralis grew under the

closed B. davidii canopy where light levels were low yet soil moisture and nutrient were

higher than on the exposed floodplain. Granted, this study utilized cultivated transplants

that had been reared in a nursey thereby limiting the conclusions that can be drawn. It

136

Reproduced with permission ot the copyright owner. Further reproduction prohibited without permission. will be interesting to learn, through future research, the influence of B. davidii on other

native species throughout their life cycle. In particular what are the interspecific

interactions between G. littoralis and B. davidii among successional stages? In the next

chapter competition between B. davidii and G. littoralis among successional stages was

examined (Chapter 5).

137

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Table 4-1. Tests of Discriminant Dimensions of the developmental stages o f Buddlej a

davidii floodplain plant communities.

Canonical Canonical Multivariate df, df2 P

Dimension Com. F

1 0.94 31.16 6 70 <0.0001

2 0.54 10.64 2 36 0.0003

Table 4-2. Standardized discriminant coefficients of attributes used to classify

developmental stages of Buddlej a davidii floodplain plant communities.

Canonical Dimension 1 Canonical Dimension 2

Light transmission (%) 0.77 0.59

Buddleja davidii biomass -0.51 0.48

Buddleja davidii age -0.59 -0.55

138

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Table 4.3. ANOVA results for response of Griselinia littoralis transplant by stage, river and stage x river. Degrees of freedom (df), MS residual, F-ratios and P-values from type III sum of squares for each ANOVA are shown. The appropriate transformation, if needed, for each response variable is shown. Response Source D f VMS residual F-ratio P=Value Variable Griselinia littoralis shoot biomass [g) (n=16) Stage 2 3.98 6.88 0.0116 River 1 8.90 15.38 0.0024 River x Stage 2 7.78 13.43 0.0011 LoglO(Aheight; cm) (n=23) Stage 2 0.74 13.74 0.0002 River 1 0.07 1.32 0.2563 River x Stage 2 0.04 0.82 0.4578 LoglO(Gme//«w littoralis SLA; g cm^) (n=18) Stage 2 0.08 36.26 <0.0001 River 1 0.01 3.06 0.1037 River x Stage 2 0.00 0.74 0.1943 Log 10( Grisel inia ittoralis root biomass (g) (n=25) Stage 2 0.49 9.33 0.0004 River 1 0.25 4.75 0.0340 River x Stage 2 0.12 2.37 0.1039 Griselinia littoralis Root: Shoot Ratio (n=25) Stage 2 0.16 19.86 <0.0001 River 1 0.04 5.39 0.0244 River x Stage 2 0.01 1.52 0.2288

139

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Sucoesskral stages Bi/dUR^dominanlnd piantaxninunfty

Upland vegetation

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Figure 28. Schematic of Griselinia littoralis transplant experiment. Griselinia littoralis was planted in 3 x 3 m plots that represented a three-stage developmental chronosequence of Buddleja davidii-àormnaXQà plant communities on South Island, New Zealand floodplains.

141

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Figure 31. Griselinia littoralis shoot biomass (y) by developmental stage (x) by river (x) after 76 wks in Buddleja <7ov/V7//-dominated stands. Stages are O = Open, Y=Young and V=Vigorous. When the error bars (95% confidence limits of the mean) overlap there was no significant difference between the rivers, stage or both.

144

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 1 2

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Figure 32. Griselinia littoralis growth (A height cm) (y) by developmental stage (x) by river (x) after 76 wks in Buddleja davidii-àovdmaXQà stands. Stages are O = Open, Y=Young and V=Vigorous. When the error bars (95% confidence limits of the mean) overlap there was no significant difference between river, stage or both.

145

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Figure 33. Griselinia littoralis specific leaf area (cm^ g ’) (y) by developmental stage (x) by river (x) after 76 wks in Buddleja davidii -dominated stands. Stages are O = Open, Y=Young and V=Vigorous. When the error bars (95% confidence limits of the mean) overlap there was no significant difference between stage, river or both.

146

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Figure 34. Griselinia littoralis root biomass (g) by stage by river after 76 wks in Buddleja (7a vf (7; ; -dominated stands. Stages are O = Open, Y=Young and V=Vigorous. Overlap of the error bars (95% confidence limits of the mean) indicate there was no statistical difference between rivers, stages or both..

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Figure 35. Griselinia littoralis root to shoot biomass ratio(y) by developmental stage (x) by river (x) after 76 wks in Buddleja c/av/c/zi-dominated stands. Stages are O = Open, Y=Young and V=Vigorous. When the error bars (95% confidence limits of the mean) overlap there was no significant difference between stage, river or both.

148

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 5

PLANT COMPETITION DURING SUCCESSION

BETWEEN AN INVASIVE,

BUDDLEJA DA VIDII AND

A NATIVE,

GRISELINIA LITTORALIS

Abstract

Buddleja davidii, an invasive shrub native to China, may be changing plant

community composition over time on braided river floodplains in New Zealand. Because

of B. davidii’s vigorous growth, slower-growing native species (e.g., Griselinia littoralis)

may be suppressed by established B. davidii, therefore altering successional trajectories.

I examined the effect of B. davidii on G. littoralis in a competition experiment under

controlled conditions. Buddleja davidii and G. littoralis cuttings were planted two per

pot in intra- and inter-specific combinations then exposed to three light levels and four

nutrient levels. These light levels approximated light availability in plant communities

that represent the three-stage developmental chronosequence of B. davidii (i.e, open,

young and vigorous stages) on New Zealand floodplains. Results of the experiment

demonstrated that G. littoralis growth was suppressed by B. davidii in the open and

young successional stages yet G. littoralis mortality was not impacted by B. davidii.

However, the influence that B. davidii had on G. littoralis was reduced in the relative

149

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. darkness of the simulated vigorous successional stage. Buddleja davidii was not affected

by G. littoralis in the open successional stage. These results demonstrate that B. davidii

does negatively affect the native community in early primary succession, yet suggest that

as succession proceeds, B. davidii cannot tolerate the low light conditions of the closed

canopy. What is key to our understanding of the role of an invasive species in dynamic

environments is that B. davidii's dominance was transient, contingent upon the conditions

being favorable. The ecological impact of B. davidii is not a long-term threat to the

native species that are able to tolerate a broader range of conditions.

Introduction

Biotic invasions are widely recognized as major threats to biodiversity and ecosystem

stability (Wilcove et al. 1998, Mack et al. 2000, Hassan et al. 2005). In many cases

native vegetation bas been temporarily or permanently replaced by non-indigenous

opportunists (Richardson et al. 2007). The order in which species are introduced and

replaced and the resultant species interactions do play important roles in structuring plant

communities (Holdaway and Sparrow 2006). Species replacement, through succession,

is driven by the propagule pool (Thompson et al. 1997), availability of suitable

germination and establishment habitat (Walker et al. 2006), resource availability

commensurate with plant needs (Ehrenfeld 2003), regulating feedback effects and chance

(Walker and del Moral 2003). Consequently, the introduction of a new species into the

system may temporarily and/or permanently alter the trajectory of plant succession.

In New Zealand, the recently denuded areas of the floodplains are characterized by

low levels of soil nutrients and a relatively slow rate of native species recruitment

150

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. (Wardle 1991). Succession of the native plant species, adapted to the low nutrient

availability, traditionally progresses from an early pioneer state colonized primarily by

dicot herbs to a secondary community of monocot herbs (Baylis 1961, Wardle 1991).

Eventually the canopy closes as woody shrubs and trees mature (Wardle 1991, Gibb

1994, Williams and Wiser 2004). The successional gradient, from open floodplain to

closed canopy forest, can be defined by the developmental stage of the stand, where the

pattern of change is induced by colonization of an open area (‘open’ stage), developing

first as clusters of young shrubs and trees (‘young’ stage) and then later into dense stands

of vegetation (‘vigorous’stage; Burrows 1991, Bellingham et al. 2001, Bellingham et al.

2005).

The majority of plant species in New Zealand are perennial and relatively slow-

growing species compared to the vegetation of temperate climates (Allen and Lee 2006,

van der Veken et al. 2007). Within the past 200 years, non-indigenous invasives readily

colonize recently disturbed floodplains, often exceeding the natives in numbers of species

and final height and density and have practically ousted the native plants from low-land

floodplains (Wardle 1991). The non-indigenous species often grow faster than the native

pioneer species yet the non-indigenous species are generally shade-intolerant, suggesting

that despite their rapid colonization following flood disturbance, they may be short term

inhabitants of the floodplain (Williams 1979, Smale 1990).

Introduced to New Zealand in the early 1900s as a garden plant, Buddleja davidii

Franchct (Family Buddlejaceae), is an aggressive invasive that forms monocultures in

floodplains and other disturbed environments (Williams 1979, Smale 1990, Gibb 1994,

Bellingham et al. 2005, Chapter 2). The impact of its dominance on native plant

151

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. succession is unknown. In order to address the question of how B. davidii might alter

succession I studied the impacts of B. davidii colonization on a native shrub Griselinia

littoralis Raoul Choix (Family Griseliniaceae) using shadehouses as successional analogs

that represented three different developmental stages (three light levels). I also included

a full factorial addition of fertilizer.

I specifically asked the following questions: (1) In the early stage of succession, what

is the impact of a non-indigenous species on a native species or the converse, what is the

impact of the native species on the non-indigenous? In other words, is G. littoralis

suppressed by the presence of B. davidii and is B. davidii affected by the presence of G.

littoralis in the open stage of development? (2) Does the impact of a non-indigenous

species on a native species continue into later stages of succession? In particular, are B.

davidii's performance and its influence on G. littoralis reduced as the community

develops a dense canopy?

Methods and Statistical Analysis

This experiment was designed to examine the interaction of stem cuttings of B.

davidii and G. littoralis under light conditions that simulated open, young and vigorous

developmental stages of B. davidii stands in New Zealand floodplains (Fig. 36). The

developmental stages were represented by different light levels created by optically

neutral shade cloth that reduced ambient light to 90, 27 and 10% of ambient light

henceforth light treatment is referred to as stage). In the young stage ambient light was

reduced to 27%, simulating light under a young B. davidii canopy on a floodplain. In the

vigorous stage ambient light was reduced to 10%, simulating the light levels beneath the

152

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. understory of woodland made up of B. davidii and other species (Fig. 37). Cuttings from

each species were planted either as same-species pairs in one pot or as one cutting of each

species paired in a pot. The pot treatments were named GG for G. littoralis grown with

G. littoralis, BB for B. davidii grown with B. davidii and either, BG for B. davidii grown

with G. littoralis or G. littoralis grown with B. davidii. The split-split plot design was:

three stages (main effects) x four nutrient treatments (described below; subplot) x three

pot treatments (split) with three replicates arranged in two blocks, yielding 216 plants per

species (total = 432; Figs. 36 and 37).

The cuttings were collected in situ from healthy plants in the austral spring of 2004.

Griselinia littoralis cuttings were collected from the Kowhai River floodplain (Fig. 38;

East Coast, South Island, New Zealand; Easting 2555953 Northing 5874637; New

Zealand Map Grid) on 23 September 2004. B. davidii stem cuttings were collected from

Conway River floodplain (Figure 48; East Coast, South Island of New Zealand, Easting

2546480 Northing 5844107; New Zealand Map Grid) on 20 October 2004. Each cutting

was trimmed of proximal leaves (and leaf scars in the case of G. littoralis-. White &

Lowell 1984) leaving either two whole or partial leaves on the distal ends of the G.

littoralis stem or two to four leaves on the distal end of the stem of the B. davidii.

Cuttings from both species were dipped in rooting hormone, lOg/liter gamma indole-3

butyric acid (Liba 10,000 Root Promoting Compound, Taranaki Nuchem Ltd, New

Plymouth, New Zealand), planted in perlite, and placed in a mist house. After 43 (5.

davidii) and 70 (G. littoralis) days, ten plants were harvested from each species to

determine the extent of root development. Each B. davidii had a well developed network

153

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. of healthy roots extending through the bottom of container. Each G. littoralis cutting had

a primary root 3 -5 cm in length.

Before transplanting, roots were washed clean and the roots and shoots were trimmed

to a uniform size within species (initial transplant dry mass in grams; mean ± SE of dried

biomass at start (Ws), n = 18: G. littoralis: roots, 0.0128 ± 0.0043; shoots, 0.3911 +

0.0262; n - 18:5. davidii: roots, 0.0850 ± 0.0309; shoots, 0.4344 ± 0.0712). The plants

were randomly assigned to 2.5 L pots containing river sand (15% fine sand: 85% very

coarse sand 2-5 mm diameter) from the Waimak River, North Canterbury, South Island,

New Zealand. One-third (36) of the 108 pots received 5. davidii congeners, one-third of

the pots received one of each species and the remaining one-third of the pots received G.

littoralis congeners. The pots were kept in a screen-house from 2 December 2004 to 8

February 2005 and were watered to field capacity with tap water twice weekly to adjust

to transplanting.

After 68 days the potted plants were moved to mini-shade houses (1.5 m x 1.2 m x

0.8 m frame covered with different densities of shade cloth. Fig. 37). There were two

shade houses per successional stage (Fig. 36). The pot locations were randomized and

the pots rotated every month within each mini-shade structure. The fertilizer treatments

were nitrogen (N), phosphorus (P) and all other nutrients (including micronutrients but

excluding N and P) in factorial combinations (henceforth called -N-P for no N or P

added, +N+P for both N and P added, +N-P for N yet no P added and -N+P for P without

N added). Plants were watered to field capacity with tap water as needed for the first 30

days. Then they were treated twice a week with 200 ml of one of four nutrient treatments

containing either N ( N H 4 N O 3 ,2 mM) and P (Na2HP04 • 2H20,1 mM), N without P, P

154

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. without N or no N or P, all mixed with a base nutrient solution containing Na 2 H P O 4 • 2

H 2 O , .25 M; K 2 S O 4 , .50 M; MgS 04 • 4 H 2 O , 1 M; and CaCh • 2 H 2 O , .5 M and Fe chelate

EDTA, 20 mM; MnS04 , 10 mM; H 3 B O 3 , 5 mM; ZnS04 , 1 mM; H 2 M 0 O 4 , 1 mM and

CUSO4 5FI2O, 1 mM. Plants that died within the first 14 days of nutrient application,

were replaced with plants of similar size and root development. The last nutrient

treatment was applied on 14 November 2005.

All plants were harvested in mid-November 2005 over seven days, approximately 250

± 3 days after the first nutrient treatment. Leaves, stems and roots of each cutting were

separated and their dry mass determined. Relative growth rate of shoots an droots of all

surviving plants were determined by the method of Hunt (1980); shoot and root RGR

(shoot = s or root =r) = [In Wf - In Ws]/At in which Wf is the shoot or root dried

biomass at final harvest, Wg is the shoot or root dry biomass at the start of the

experiment, and At (250) is the time from start until harvest (Hunt 1980). From these

measurements I calculated root to shoot biomass ratios. I calculated total leaf area on

fresh leaves from each cutting using a scanner and WinFOLAR computer image analysis

software (Regent Instruments, Inc., Quebec City, Quebec, Canada). Leaf area was used

to calculated specific leaf area (i.e., a measure of leaf density and thickness; SLA=total

leaf area/total dry leaf mass). Foliar N and P were measured on 0.2 g of leaf material

(which included petioles) from each seedling that were digested in acid prior to

colorimetric analysis (Alpkem 1992, Alpkem Corporation, Oregon, USA) and reported as

mg g ' of dried leaves per plant.

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Statistical analyses

Six response variables were used in this study; shoot relative growth rate (SRGR),

root relative growth rate (RRGR), root to shoot biomass ratios, specific leaf area, foliar N

and foliar P. To meet the assumptions of normality and homogeneity in error, values

were transformed. Shoot and root relative growth rates were calculated from the natural

log of shoot and root biomass. The remaining response variables were transformed as per

Box and Cox (1964); the root to shoot biomass ratios were transformed using the

equation [log (root: shoot) * 0.35]; specific leaf areas were transformed using the equation

[(SLA-0.2 -l)/-0.00053]; foliar N was transformed using the equation [(N 0.4-1)70.16]

and foliar P was transformed using the equation [(P-0.2 -1)7-0.10]. Diagnostics revealed

that there were eleven specific leaf area values that were influential outliers (values >1.5

of the interquartile range with standardized scores > 3.29; Tabachnick and Fidell 1996).

When data transformation did not correct the influence of the outliers, values one unit

greater than the most extreme, non-outlier score were substituted for the deviants

(Tabachnick and Fidell 1996). Transformations (Box and Cox 1964) and adjustment of

influential values satisfied the assumptions of normality, homogeneity of variance-

covariance matrices, linearity and multi-collinearity (Tabachnick and Fidell 1996).

After data transformation and adjustment the data was further corrected for an

unbalanced design. The actual experiment was conducted such that there were six pots

with two of the same species cuttings per pot treatment (for a total of 12 replicates per pot

treatment). However, there were six pots with one cutting of each species per treatment

(for a total of six replicates per species per pot treatment). Consequently, I had an

unequal number of replicates for comparison. To correct this error, the total number of

156

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 432 specimens was reduced to 288 with the random selection (per each stage by nutrient

by same species treatment) and removal of half of the plants from the same species pots

resulting in six replicates of each species per treatment.

Contingency table analyses using Chi-Square tests were performed to test for

independence of mortality and light, nutrient and pot treatments (plants were considered

dead when there was no evidence of aboveground living tissue). Pretreatment

comparisons between species were compared using separate t-tests on shoot and root

biomass and foliar N and P concentrations (SAS PROC TTEST, SAS 9.1, SAS Institute

Inc, Cary, NC, USA). Separate split split-plot design analyses of variance (ANOVA)

were used to analyze treatment responses of the experiment (e.g., changes in species).

The main effects were light split into four sub-plots by nutrient treatment. The nutrient

sub-plots were further split into four pot treatments (Fig. 37). When these effects were

significant (P<0.05), Tukey’s multiple comparison tests of the least square means were

used to compare light, nutrient, and pot treatments (PROC GLM; SAS 9.1, SAS Institute

Inc., Cary, NC, USA).

Results

Survivorship was high for both G. littoralis and B. davidii irrespective of pot

treatment (< 6% [25 plants] died during the experiment). B. davidii plants in the vigorous

stage accounted for 48% of the mortality between the two species and across the three

light treatments (Fig 39;f = 0.0361, = 18.48, df = 2). Survival was not significantly

affected by nutrient treatment (Fig 39; -N-P: 0.93%; +N+P: 1.62%; +N-P: 0.93%; -N+P:

157

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 2.31%; P = 0.2406, = 4.20, df = 3;) or pot treatment (Fig.39; GG: 4.17%; GB: 0.93%;

P = 0.2739, = 1.20, df = 1; BB: 4.63%; BG: 1.85%; P=0.6959, = 0.15, df = 1).

Three-way MANOVA confirmed the main effects of light, nutrient, and pot treatment

(FT) on the six response variables; shoot relative growth rate (SRGR), root relative

growth rate (RRGR), root:shoot ratio, specific leaf area (SLA) and foliar nutrient

accretion. There were significant two-way interactions (light x PT, nutrient x FT,

nutrient x light). The three-way interaction (lightxnutrientxFT) was not significant (F =

0.4711, Wilks’ Lambda F = 1.01, df = 90,159.75) and thus, was excluded from the

general linear model. In addition, there were no block effects at any level of the model.

Fretreatment condition

The pretreatment shoot biomass values of B. davidii and G. littoralis were not

significantly different, however, B. davidii root biomass was ca. seven-fold greater than

that o f G. littoralis (ts4=2.31, P=0.0332). Fretreatment comparisons oïB. davidii and

Griselina foliar N and foliar F concentrations were conducted in order to determine

whether B. davidii foliar nutrient concentrations were inherently different than those of

G. littoralis. Fretreatment B. davidii foliar N and F were 3.13 and 3.40 times greater than

that o f G. littoralis (foliar N: t34=8.67; P <0.0001 ; foliar F:t34=10.43; P <0.0001).

Impacts of Treatments

Summary

There was an approximate 17-fold increase in B. davidii biomass from the start of the

experiment until it ended, whereas G. littoralis biomass increase was less than two-fold.

Buddleja davidii and G. littoralis root biomass increased 27- and 22-fold, respectively.

Fost-treatment, B. davidii nutrient concentration continued to be greater than those of G.

158

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. littoralis (foliar N \B. davidii ca. two-fold greater than G. littoralis\. t274=9.1I, P<0.0001 :

foliar P: [B. davidii ca. 1.05 times greater than G. littoralis]-. t253=14.55, P<0.0001).

Griselinia littoralis was negatively influenced by the presence of B. davidii

(Table 5-1). Shoot and root relative growth rates were the least in the vigorous stage,

greatest in the young stage (Table 5-2; Figs. 40a-b) and root to shoot ratios were greatest

in the open stage for both species (Table 5-2; Fig. 40c). Specific leaf area was greatest in

the vigorous stage for both B. davidii and G. littoralis (Table 5-2; Figs 40d-e). However

G. littoralis did not accumulate foliar N and P in the vigorous stage as did B. davidii

(Table 5-2; Fig 401).

Whether species were sensitive to nutrient manipulations was dependent upon stage

(i.e., stage x nutrient interaction; Table 5-3) and the species of the neighboring plant (i.e.,

plant treatment x nutrient interaction; Table 5-3). There were significant stage x nutrient

interactions that accounted for differences in the above- and below-ground growth rates,

specific leaf area and foliar P (Table 5-3) and plant treatment x nutrient interactions that

accounted for differences in the above- and below-ground growth rates and foliar P yet

not SLA (Table 5-3; see “Impacts of Nutrients x Stage x Pot treatment” section below for

the results per least square means comparisons).

Impacts of Nutrient by Stage per Pot Treatment

The addition of N and P in the open and young stages dramatically increased above-

and below-ground growth rates in B. davidii {P <0.001) yet not in the vigorous stage

(Figs. 41 and 42) despite whether the neighboring plant was a congener or G. littoralis

(Henceforth the P-values of significant responses are reported as P <0.05, 0.01 or 0.001,

as appropriate, and the actual LS means per nutrient by stage by plant treatment treatment

159

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. and P-values are reported in Appendix VI). The addition of N and P caused a slight

increase in the rate of shoot and root growth in G. littoralis however rates were not

significantly different than when nutrients were withheld (Figs. 41 and 42). Regardless

whether nutrients were added or omitted the presence of B. davidii suppressed Griselina

shoot and root growth rate in the open and young successional stages in comparison to

the G. littoralis grown with its congener (Fig. 41 and 42, P<0.01). However, B. davidii

did not affect the above- and below-ground growth rates of G. littoralis in the vigorous

stage despite the nutrient treatment.

Root to shoot ratio was greatest in the open and young stages when neither N nor P

were added to either species (Fig 43, f<0.001). This is particularly noteworthy because

the -N-P nutrient treatment was designed to simulate the conditions of a recently

disturbed floodplain (see Chapter 3). The converse was the case in the vigorous stage,

when nutrients were withheld, the root to shoot ratio was the least, yet the differences

were not significant (Fig. 43). The addition of both nutrients together suppressed the root

to shoot ratio, more notably in G. littoralis than in B. davidii (Fig. 43, P<0.001). The P-

only treatment promoted G. littoralis root development (relative to shoot development) in

all three stages, yet most significantly in the vigorous stage (Fig. 43, P<0.001).

Neither species increased leaf area in response to the addition or omission of nutrients

(Fig. 44). The impacts of adding nutrients to B. davidii were detected in foliar N and P

concentrations particularly in the vigorous stage (which was associated with B. davidii's

increase in specific leaf area in the vigorous stage; Figs. 44-46). Note how responsive B.

davidii was to the omission of P and the omission of N compared to the response of the

other cuttings (Figs. 45-47, P<0.001). These responses indicate that B. davidii nutrient

160

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. uptake is commensurate with availability (Clarkson 1985). Foliar N and P concentrations

in G. littoralis were not as notable, except for a spike in N concentration in the N only

treatment in the young stage when grown with B. davidii (Fig. 45, P<0.05). This spike

was not evident in G. littoralis grown with its congener (Fig. 45).

Discussion

Results of my experiment show that G. littoralis growth was suppressed by B. davidii

in the experimental conditions analogous to the open and young successional stages of a

New Zealand floodplain (Figs. 41, 42 and 46) yet G. littoralis mortality did not increase

in the presence of B. davidii (Fig. 39). However, the influence that B. davidii had on G.

littoralis was reduced in the relative darkness of a simulated vigorous stage of succession

(Fig 40). These results demonstrate that B. davidii can potentially have a negative effect

on the native community after disturbance, yet also suggest that eventually B. davidii will

decline when it can no longer tolerate the low light conditions created by the closed

canopy.

Previous studies conducted in New Zealand floodplains found that when present, B.

davidii will dominate in early succession (Williams 1979, Smale 1990, Wardle 1991,

Gibb 1994, Bellingham et al. 2005). In the Urewera National Park, North Island, New

.Zealand, native plant species were suppressed by B. davidii in the absence of

anthropogenic or natural disturbance (William 1979) and 5. davidii displaced primary

native colonizers where it occurred en masse (Smale 1990). Immediately following a

disturbance in the floodplain (whether due to a flood or excavator) B. davidii dominated

early succession on the Kowhai River, South Island, New Zealand (Bellingham et al.

161

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 2005). Buddleja davidii's, influence over G. littoralis in the shade house experiment is

comparable to B. davidii'% dominance on the floodplain after flooding.

Buddleja davidii has several traits that contribute to its temporary dominance. It

grows more rapidly than most New Zealand natives including G. littoralis (Baylis 1959,

Dansereau 1964, Williams 1979, Smale 1990, Williams and Wiser 2005). Buddleja

davidii can increase 0.5 m in height annually and seedling stem diameter can increase

annually by 1 cm year ' in the United Kingdom (Miller 1984). Owen and Whiteway

(1980) in the United Kingdom, reported that B. davidii on building rubbish heaps grew to

2 m and flowered in one season and then within the next three to four years formed an

extensive bush more than 4 m high. I found that, although the cuttings of both species

were comparable in the beginning, B. davidii biomass increased 17-fold in ca. 250 days

while G. littoralis biomass increase was less than 2-fold greater in the same period.

Light availability is elearly an important driver for B. davidii success as a dominant

colonizer. As the canopy develops intense self-thinning occurs over the first few years

(Williams 1979, Smale 1990, Bellingham et al. 2005) with stand densities declining from

as many as several million plants ha ' in a one yr-old population to ca. 13,000 plants ha '

in 3-5 yr-od stands (Smale 1990). Furthermore, self-thinning is complete after 10 yrs

when B. davidii density has dropped to 2500 plant ha ' (Smale 1990). In addition, B.

davidii seedlings were not found beneath the mature forest canopy in New Zealand

(Brown 1990, Chapter 4), North America (per. obs.) or United Kingdom (Miller 1984).

Buddleja davidii seeds require full sun to germinate (Miller 1984; Brown 1990, Wilson et

al. 2004), consequently the absence of B. davidii seedlings has been attributed to B.

davidii'?, low tolerance for shade, not allelopathy (Miller 1984).

162

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Phenotypic plasticity under different conditions can influence the impact of a

dominant species on the plant community as a whole (Daehler 2003). Buddleja davidii is

characterized by a highly plastic phenology (Miller 1984, Feng et al. 2007; Ebeling

2008). Phenotypic plasticity following nutrient application was evident in this study (Fig.

46). Buddleja davidii was the least robust in the no nutrient added treatment (-N-P; first

pot on the left in Fig. 46) and the most robust in the full nutrient addition treatment

(+N+P). Buddleja davidii shoot growth rate was the same for both the +N-P and -N+P

treatments. Still, B. davidii treated with +N had many branches in comparison to +P

treatment which were were unbranched (Fig. 47). Based on the response of the -N+P

treatment, I suggest that when the stems are linear, with little branching, more light can

pass through the canopy and thus promote growth in the understory. We observed

various growth forms of B. davidii in New Zealand fioodplains (see Chapter 3) where the

size, branching and shape of B. davidii differed dramatically depending upon soil

fertility, substrate type, soil moisture and light levels (pers. obs.).

Successful invasive species must use limited resources more efficiently than native

species (Vitousek 1986). Furthermore, when invasive species have higher growth rates

and photosynthetic values than native species they may have ecophysiological traits that

increase resource capture and utilization efficiency (Pattison et al. 1998). Although the

parent plants from which B. davidii originated were cultivated for nutrient rich conditions

found in gardens they grew remarkably well in low nutrient soils (Humpheries and

Guarino 1987, Gillman et al. 1998, Feng et al. 2007) and had a significantly higher

resource capture ability and utilization efficiency with higher N allocation to the

photosynthetic machinery than native woody species in Europe (Feng et al. 2007). On N-

163

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. poor soils in the United Kingdom, B. davidii can out compete Betula pendula (Humphries

and Guarino 1987). This study has shown that regardless of soil fertility, N and P foliar

concentrations of B. davidii were significantly greater than in G. littoralis especially in

the vigorous successional stage.

Scavenging nutrients may be more costly than beneficial to plants (Chapin 1985).

Native species that evolve in low-nutrient environments do not usually benefit from

excess nutrient availability (Baylis 1961, Wardle 1991). Buddleja davidii àQvaonsXxaXQà

dramatic luxury consumption of nutrients in response to nutrient additions and omissions

(Figs. 45 and 46) even though B. davidii leaves have inherently higher concentrations of

N and P than many woody species (Comelissen et al. 1997, Bellingham et al. 2005, Feng

et al. 2007, Thomas 2007). The cost of such rapid nutrient uptake to B. davidii is

unknown.

Mycorrhizae fungi, as in the case of B. davidii (Dickie et al. 2007) and G. littoralis

(Baylis 1959, 1961) facilitate the plants uptake of soil P, especially in low fertility

systems. However, the strongly mycotrophic G. littoralis littoralis responded only

weakly to added F in this and other studies (Bellingham et al. 2003, Walker et al. 2003),

which suggests that its mycorrhizal system and growth rate are adapted to low

concentrations of available P as found in native New Zealand soils (Baylis 1959). In

contrast, I found in this study that 5. davidii's uptake was commensurate with the amount

of P added or withheld.

The long-term impact of B. davidii sequestering P in natural systems has not been

directly addressed. I detected parallel patterns between soil P and B. davidii biomass

over time suggesting that soil P concentrations increased and decreased comensurate with

164

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. the rise and fall of 5. davidii biomass over a 10 year period (Chapters 3 and 4).

Theoretically, if B. davidii sequesters P than P may become unavailable to the slower

growing native species. This may lead to altered successional trajectories (Bellingham et

al. 2005). Conversely, as a semi-deciduous species, B. davidii potentially could enrich

soil fertility over time if B. davidii does not remobilize N and P before biannual leaf

abscission. Even if 5. davidii efficiently remobilizes nutrients, leaf litter must be

enriching the soil.

Bellingham and others (2005) determined that organic soil N under mixed woody

stands (that included B. davidii) was two times greater than under younger woody stands

and mineral soil N under mature mixed stands was more than twice that measured under

mature monocultures of Coriara arborea stands in New Zealand. Furthermore, the

decomposition rates of congeneric B. asiatica in Hawaii increased soil fertility (Matson

1990). 1 found that the presence of B. davidii increased root growth in G. littoralis (Fig.

42). However, the mechanisms contributing to and consequences of the enhanced growth

are areas needing additional research.

This study provides strong evidence that even though B. davidii initially dominates

the floodplain plant community, its influence may be temporary because it can not

tolerate the closed canopy community of the later stages of succession on New Zealand

fioodplains. Native speeies, able to tolerate a broader range of conditions dominate the

later stages of succession.

165

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Table 5-1. Buddleja davidii and Griselinia littoralis cutting response variables from shade house experiment and their relationship among plant treatment presented in descending order of least square means (Tukey adjusted for multiple comparison). P values < 0.05 are denoted as >. BB=Two Buddleja davidii per pot BG or GB=One Buddleja davidii and one Griselinia littoralis per pot GG=Two Griselinia littoralis per pot Shoot Relative Growth Rate BG>BB>GG>GB

Root Relative Growth Rate BG >GG=BB>GB

Root to shoot biomass ratio GB>GG>BB=BG

Specific Leaf Area BB=BG>GB>GG

Foliar N concentrations BG=BB>GG=GB

Foliar P concentrations BG=BB>GG=GB

Table 5-2. Stage by plant treatment response variables oiBuddleja davidii and Griselinia littoralis cutting response variables from shade house experiment presented in descending order of least square means (Tukey adjusted for multiple comparisons). P values < 0.05 are denoted as >. BB=Two Buddleja davidii per pot BG or GB=One Buddleja davidii and one Griselinia littoralis per pot GG=Two Griselinia littoralis per pot Shoot Relative Growth G G young ~ G G o o en ^ GB young ~G G vigorous ~GG onen ~ GByigorous Rate BGyoung ~ B G open ~BBvoung ~ BBppen “ BGyjgorous ^ BByjgorous Root Relative Growth G G young ^ G B open ~ G B young “ "G G open ^ GGyjgorous ~ GByigorous Rate BGopen~BGyoung~BByoung BBopen ^BByjgorous ~ BGyjgorous Root to shoot biomass GBopen^GByoung~GGyoung~GGopen^ GGyigorous""G Byjgorous ratio B B open “ BGppen ~BByoung ~ B G young ^ BByjgorous ~ BGyjgorous Specific Leaf Area GByjgorous~GGyjgorous^GByoung~GBopen~GGyoung~GGopen BGyjgorous^BByigorous^BBooen~BGyoung~BByoung~'BGooen Foliar N GGyoung~GGopen~GByjgorous~GGyjgorous~GByoung'~GBooen concentrations BByjgorous~BGyjgorous^BGyoung~BBopen~BByoung~BGopen Foliar P GGyoung~GGopen GGyjgorous^GByjgorous GByoung“ GBopen concentrations BGyjgorous BByjgorous^BGyoung~BByoung~BBooen“ BGopen

166

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168

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Figure 37. The three-stage (i.e., open, young and vigorous) developmental chronosequence (time since disturbance by flooding) in Buddleja <7avi<7//-dominated plant communites and their shade house analogs based upon conditions found on New Zealand fioodplains. Griselinia littoralis and Buddleja davidii were grown for ca. 251 days, planted with either their congeners or the other species under three light levels and with and without additions of nitrogen, phosphorus or both added twice weekly to the sand- gravel mix in each pot as described in Fig. 36.

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Figure 40. Plots of means and 95% confidence limits of pooled data of Buddleja davidii and Griselinia littoralis cutting response variables presented by developmental stage (%; i.e., open,young and vigorous) and plant treatment (without consideration for nutrient treatment). 7-axis are (a) shoot relative growth rate (g d '), (b) root relative growth rate (g d'') (c) root to shoot biomass ratio (d) specific leaf area (cm^ g ') (e) foliar N (%) and (f) foliar P (pg g''). The plant treatments are represented by different line types as described in the figure legend; BB=Two Buddleja davidii per pot, BG or GB-One Buddleja davidii and one Griselinia littoralis per pot, GG=Two Griselinia littoralis per pot.

172

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 6

CONCLUSIONS

The studies presented in this dissertation address a variety of questions on how an

invasive plant species impacts plant succession. Species recruitment, establishment, and

senescence are the functions of the additive effects of the abiotic conditions and biotic

interactions (abiotic: i.e., soil chemistry, catchment climate; biotie: herbivores,

mutualists, competitors; Mitchell et al. 2006). These studies of the impact of B. davidii

on New Zealand floodplain plant communities and ecosystem properties, and the

interactions between B. davidii and G. littoralis present evidence that B. davidii has the

capacity to alter successional trajectories by changing community composition and

modifying biogeochemical cycles.

Seasonal floods scour the riverbeds, remove the vegetation and reshape the

fioodplains and active river channels (Gray and Harding 2007). As a result, the

fioodplains are ideal B. davidii habitat. Buddleja davidii quickly dominates the exposed

substrate by way of high seed production over a period of 2-3 months armually;

(Lockwood et al. 2004, Chapter 2). The length of time that B. davidii is dominant is

relatively short: however, during this time, the species may facilitate subsequent species

(native and non-indigenous) recruitment by adding P to the soils and increasing structural

diversity (Chapter 3 and 4). Buddleja davidii'?, dominance is short-lived because it is

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. shade intolerant. Nevertheless, B. davidWs impact on succession may have long-term

effects.

The fioodplains on the South Island of New Zealand shifted from relatively

unvegetated to dense stands of woody plants in less than 10 years (Chapters 3 and 4).

The developmental trajectory of the B. r/av/J/i-dominated communities progressed from

open bare soil to native and non-indigenous forbs (e.g., native: Roulia spp., non-

indigenous: Trifolium spp.) and grasses (e.g., native: Cortaderia richardii, non-

indigenous: Holcus lanatus) to woody shrubs and trees (e.g., native: Coriaria spp., non-

indigenous: Salix spp.); however, B. davidii cover was often 20 times greater than that of

any other species, native or non-indigenous. Only 8.57% of the other species present

(i.e., native and non-indigenous) contributed > 3% of the total vegetative cover. Several

native forbs and grasses (e.g., Epilobium spp., Raoulia spp., Cortaderia spp.), which are

generally found on fioodplains not invaded by B. davidii, had low frequency of encounter

(< 2%) and had low cover (< 3%). Buddleja davidii dominated the open, young, and

vigorous stages (0-8 yrs after flooding) on exposed floodplain, within channel islands,

and on the edges of riparian terraces habitat. The species declined in cover in the mature

stages. The presence of mature B. davidii shrubs on the fioodplains was ca seven times

less likely than in the three other stages combined and was restricted to the edges of

riparian terraces. Native shrubs and trees were present in all four stages as seedlings,

saplings, and adults; however, in negligibly low frequencies (no species occurred in > 6%

of the plots) and had an average cover of < 3%. An exception to this is Coriaria arborea,

which was found in 20% of plots with an average cover of 37.5 ± SE 2.73%. There was a

four-fold increase in B. davidii foliar N and P concentrations along the developmental

182

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. gradient. This gradient stabilized in either the vigorous and mature stages. Soil physical

properties did not vary between stages or catchments: however, soil P and N

concentrations were positively correlated? with an increase in B. davidii biomass. This ,

suggests that B. davidii may augment soil fertility.

Chapter 3 reported that these results were consistent with Bellingham and others

(2005) and demonstrated that B. davidii can alter successional dynamics by dominating

the plant community, competing with native species, and enhancing soil fertility. My

results are also similar to those described by Williams (1979) and Smale (1990) on the

North Island of New Zealand, in Urewera National Park. Williams (1979) observed that

native species were less abundant in the presence of B. davidii. Smale (1990) determined

that B. davidii displaced the initial native woody plants often found in the early

succession (e.g., Kunzea ericoides), and accelerated succession on fresh alluvium by

replacing long-lived native forest species.

When present on a floodplain, B. davidii facilitated the recruitment and establishment

of woody species earlier in succession than is found on fioodplains that were free of 5.

davidii (Chapter 3). Griselinia littoralis growth was enhanced by the protection and

shade of the B. davidii understory (Chapter 4). The shade house experiments confirmed

that B. davidii cuttings were not tolerant of the simulated low-light conditions of mature

vegetative stands that develop on terraces and channel islands in the decades following

floods (Chapter 5). These results help explain why B. davidii is absent in the intact

upland forests (Williams 1979, Smale 1990, Bellingham et al. 2005). In addition,

although G. littoralis was suppressed by the presence of B. davidii in the early stages of

succession, B. davidii did not contribute to the mortality of G. littoralis.

183

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Management and control of non-indigenous species are critical for maintaining native

biodiversity and normal ecosystem function (Byers et al. 2002). Although some invasive

plant species have proven to be problematic (e.g., Pueraria montana var. lobata, kudzu),

the majority of invasive species (80-90%) may have only minimally detectable effects on

native communities (Williamson 1996). Non-indigenous species are established on every

landscape worldwide. Therefore, the issue of introduction and prevention of introduction

of these species moot. Consequently, ecologists and managers are forced to set priorities

for the control and containment of only the non-indigenous species that prove to be

invasive (Parker et al. 1999, Byers et al. 2002). Control and containment are best

accomplished in the early stages of introduction. Unfortunately, a time lag of several

decades or longer between initial introduction of an organism and the time it invades

natural communities makes management of invasive species difficult (Williamson 1996,

Ewel et al. 1999). In addition, the fact that most invasions are irreversible once the

invasive species has naturalized further frustrates management efforts (Ewel et al. 1999).

Succession is the process of species change over time and is directed by internal (e.g.,

biotic interactions) and external stressors (e.g., drought; Odum 1985). Invasive species

that alter biotic interactions may irreversibly change ecosystems and therefore, reduce

productivity and biodiversity of that ecosystem. Quantitative research on invasive

speeies is needed to identify the impact on the ecosystem if and when specific biomass

and frequency are low and specific biomass and frequency are high (Byers et al. 2002).

Because resources to manage invasive species are limited, managers must determine

which species and landscapes they require focused efforts. Consequently, ecologists are

tasked with determining the short- and long-term impacts of invasive species on natural

184

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. systems. In particular, they must address whether invasive species transform ecosystems

by permanently altering the normal functioning of natural systems and disproportionately

affecting native biota (Byers et al. 2002).

Recommendations for Further Study

1. Native species recruitment and establishment on New Zealand fioodplains occur

more slowly than the recruitment and establishment of dominant invasives. The

lag in recruitment by natives following floods has permitted the establishment of

invasives that have traits for rapid recruitment, establishment, and reproduction

after flooding. Within less than 200 years, some fioodplains in New Zealand have

been transformed from sparsely populated systems dominated by scattered, often

cryptic forbs and grasses (e.g., Epilobium spp., Raoulia spp.) to highly diverse

communities with showy non-indigenous plants (e.g., B. davidii, Lupinus

arboreus,Cytisus scoparius). This research and other studies have confirmed that

B. davidii has altered successional trajectories on New Zealand fioodplains;

however, the ramifications of accelerating or by-passing certain successional

stages for the native community are unknown. A recommendation for future

research is to experimentally manipulate a chronosequence of B. davidii stands in

order to force the transition of one species assemblage to another. This may,

accelerate succession and transform the ecosystem. This experiment could be

done by thinning or removing early successional species and by adding late

successional species. An experiment of this kind can could enhance our

185

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. understanding of succession and provide information on the impact of B. davidii

over time.

2. Our present understanding of the impacts of B. davidii is based upon a few

individual studies that have been conducted in particular geographic regions on

specific processes or functions. Quantitative studies in a variety of areas are

needed to determine the specific impact that B. davidii may have on key riparian

ecosystem functions and processes, such as water consumption, nutrient cycling,

wildfire frequency, and frequency and intensity of flooding. Leaeh (2007) found

that B. davidii does increase sediment accretion on the Tolt River in Washington,

USA This suggests that B. davidii may influence sediment loading and channel

formation in other areas as well. However, very little is known about how B.

davidii impacts the hydrology of other systems where it has invaded. The basis

for future research could be to distinguish which of B. davidii's impacts are

negligible (i.e., low-impact; Byers et al. 2002) and which cause major changes in

native biodiversity (i.e., high-impact; Byers et al. 2002)

3. Buddleja davidii's presence on New Zealand fioodplains increases structural

diversity of the system and alters movement of plants and animals. For example,

vigorous and mature B. davidii stands have many stems and are > 4 m tall. These

stands are attractive to birds that may drop seeds from native species such as G.

littoralis in their feces. In addition, dense stands are physical barriers in which

litter and seeds accumulate. Native plant communities on the active floodplain

were less structurally diverse. What are the cascading effects of altering the

structural diversity? Are birds dropping seeds in transient B. davidii stands that

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. would normally be dropped in upland forest? This could alter recruitment and

population dynamics of the upland forest. This is a possible avenue for future

researeh.

4. My catchment scale analyses of factors common to New Zealand fioodplains

infested by B. davidii were a first attempt at understanding the influence that the

landscape may have on the susceptibility of fioodplains to invasion by B. davidii.

An in-depth analysis of landscape attributes and their relationship to the presence

or absence of B. davidii in a catchment is needed to model system invasibility and

potential distribution. Current databases (e.g„ Department of Conservation,

National Vegetation Survey) and herbaria records provide some information

about the presence of 5. davidii', however, quantitative data about abundance and

location of 5 davidii are needed.. Why B. davidii has established in one

floodplain and not in another is still not known. This information is essential to

determine the best options for management of invaded areas and protection of

areas in which B. davidii has not yet established. Further studies could include a

comparison of the landscape attributes (i.e., land-use history, percentage of roads,

population density) along an environmental gradient among fioodplains where B.

davidii is present (e.g., the ones identified in this study) with those attributes

where B. davidii is absent (e.g., Otago-Southland). Such a study could identify

landscape-scale attributes that may facilitate or hinder B. davidii invasion (Byers

et al. 2002).

5. Current databases (e.g.. New Zealand Department of Conservation and National

Vegetation Survey) and herbaria records provide some information about the

187

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. presence of B. davidiv, however, what are needed are quantitative data about B.

davidii abundance and location. Buddleja davidii, like many invasives that

establish in heterogeneous patches on the landscape, is difficult to detect and map

using remotely sensed data such as aerial photographs and satellite imagery.

Furthermore, it is difficult to acquire imagery of floodplains located in narrow

valleys because B. davidii foliage has low contrast compared to other species.

Similar problems exist in mapping many invasive plant species that do not

dominate the canopy or establish in the understory. Recently, remote sensing has

been successfully used to map the distribution of canopy-dominating invasive

plant species (Underwood et al. 2003, Hunt et al. 2004, Joshi et al. 2004).

Indirect mapping approaches can predict the distribution of species using

knowledge about the ecological relationship between a species and its

environment (Joshi et al. 2004). Joshi and others (2006) were able to predict

cover and seed production of the shrub species, Chromolaena odorate, in the

forest understory in the Southern Himalayas using Landsat ETM+ image

processed through a neural network. Their success (89% based on forest canopy

density and 81% based on light intensity) suggests that it is feasible to map plant

species using indirect remote sensing methods. Light transmission can determine

the competitive and reproductive traits of B. davidii ; therefore, light transmission

in the riparian and fioodphnn forest may allow the distribution and reproduction

of B. davidii to be mapped. In order to develop a model of landscape invasibility,

it would be important to map B. davidii abundance and extant.

188

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 6. The general assumption is that if an invasive species has been able to gain

dominance in an area than some component of the system no longer favors the

native species, but instead favors the invasive (Davis et al. 2001). An important

part of management and control is to determine the functions and components that

have been disrupted to favor the invasive (Parker et al. 1999, Byers et al. 2002).

A retrospective analysis of catchment-scale landuse and hydrology may identify

conditions that promote invasibility.

7. Because naturalized B. davidii was derived from horticulturally selected stock, the

naturalized plants may be more vigorous than plants in the native Chinese

populations. Ebeling et al. (2008) determined that invasive B. davidii collected

from populations naturalized in Germany grew more rapidly than B. davidii plants

grown from seeds collected from natural areas in China. It is likely that humans

selected for plants that were more tolerant of a range of stressors such as cold and

drought than are native plants. Are the cultivars generally larger, taller and have

more flowers than native plants, creating “super-invaders” that are able to survive

and compete with natives? A quantitative shade house study of native,

naturalized and cultivated B. davidii could be designed that would investigate

specific tolerances to extreme conditions. Such a study could be used to develop

a model of the potential distribution of garden and naturalized seeds.

8. The current distribution of naturalized B. davidii has been linked to human

population density: the source of invasive B. davidii was individual plants that

were deliberately planted in household gardens and commercial landscapes

(Healy 1946,Williams 1979, Esler 1988, Tallent-Halsell, pers. obs.). Buddleja

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. davidii seeds are typically wind-dispersed; however, they may be transported by

water and animals. An analysis of source and satellite populations and dispersal

mechanisms could contribute to our understanding of the invasive dispersal

potential of this species. The conditions that promote or inhibit dispersal distance

of B. davidii seeds on floodplains and other disturbed areas could be measured

and models of B. davidii migration from source populations to spread across

landscapes developed.

9. Because B. davidii is shade intolerant, it does not spread into intact forests, a

feature that restricts its distribution to open areas that have been disturbed.

Worldwide, the horticultural community continues to breed B. davidii to create

new varieties (e.g., flower color, dwarfism, leaf shape, disease resistance; Wilson

et al. 2004). If a new hybrid variety were to become shade tolerant, than the

negative impact on natural habitats in New Zealand could be greater than is

currently observed. The ecological and horticultural communities must

collaborate to ensure that breeding and propagation programs do not create super

invaders.

10. Flowers have immediate and long-term effects on human emotions, moods, social

behaviors, and memory (Haviland-Jones et al. 2005). The cultural significance

ofB. davidii’s presence can not be ignored. The destruction of urban areas during

and World War II in the United Kingdom promoted the spread of B. davidii from

gardens to the debris of bombed buildings (Owen and Whiteway 1980). Buddleja

davidii’?, colorful flowers must have contrasted dramatically with the post-war

landscape, perhaps generating feelings of well-being in the local populace . For

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. this reason it seems to be difficult to convince the public to contain or remove

cultivated and naturalized B. davidii and other invasive cultivars once established

(KCGF 2007). Ecologists, land-managers and sociologists should participate in

cross-disciplinary studies into the sociological and psychological aspects of native

and invasive landscapes to address the public appreciation for B. davidii as well as

develop methods for educating the public on the detrimental effects of allowing

an invasive like B. davidii to thrive in gardens and natural landscapes.

Conclusions

Buddleja davidii has established on floodplains on the South Island of New Zealand

and total eradication of the species from these areas is unlikely. Even if policies were

implemented to restrict the further distribution of 5. davidii, its presence in gardens and

natural areas throughout the country provide a ready seed source for future invasions.

Removal efforts are labor- and resource- intense and regeneration by seed and vegetative

fragments is frequent. Biocontrol efforts may limit invasion until native communities

reestablish. In addition, B. davidii'?, presence in New Zealand is not condemned

unequivocally by the public. The species’ bright flowers are displayed throughout the

summer and early fall. They compliment the foliar display of other invasive species that

are co-dominant on some floodplains (e.g., the lavender arboreus and the yellow

of Ulex europaeus and Cytisus scoparius) and are in dramatic contrast to the less

prominent flowers of native floodplain species. There is a need to understand the impacts

that B. davidii has on ecosystems. Buddleja davidii'?, presence in natural areas may be

191

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. permanent. If so, ecologists must provide land managers with the information they need

to control and contain naturalized populations, as well as to protect native biodiversity.

192

Reproduced with permission ot the copyright owner. Further reproduction prohibited without permission. REFERENCES

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. VITA

Graduate College University of Nevada, Las Vegas

Nita Gay Tallent-Halsell

Home Address: 603 Ancient Mayan Dr. Henderson, Nevada, 89015

Degrees: Bachelor of Science, Biological Sciences, 1989 University of Nevada, Las Vegas

Masters of Arts, Science, 1998 University of Nevada, Las Vegas

Dissertation Title: Impacts of an Invasive Shrub, Buddleja davidii (butterfly bush) on Plant Succession on New Zealand Floodplains

Dissertation Examination Committee: Chairperson, Dr. Lawrence R. Walker, Ph.D. Committee Member, Dr. Stanley D. Smith, Ph.D. Committee Member, Dr. George G. Malanson, Ph.D. Committee Member, Dr. Duane A. Peltzer, Ph.D. Graduate Faculty Representative, Dr. Brenda J. Buck, Ph.D.

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