ECOPHYSIOLOGY OF BARRIER ISLAND BEACH PLANTS: RESPONSES IN FORM AND FUNCTION TO DAILY, SEASONAL AND EPISODIC STRESSES
By
THOMAS E. HANCOCK
A Dissertation Submitted to the Graduate Faculty of
WAKE FOREST UNIVERSITY GRADUATE SCHOOL OF ARTS AND SCIENCES
In Partial Fulfillment of the Requirements for the Degree of
DOCTOR OF PHILOSOPHY
in the Department of Biology
December 2009
Winston-Salem, NC
Approved by:
William K. Smith, Ph.D., Advisor
Examining Committee:
John V. Baxley, Ph.D.
Ronald V. Dimock, Ph.D.
Kathleen A. Kron, Ph.D.
Miles R. Silman, Ph.D.
ACKNOWLEDGEMENTS
I would like to thank my advisor, Bill Smith, for his untiring efforts over the past nine years of my residence here at Wake Forest University. I know that I am probably his most “untraditional” student to date. He is an exceptional scientist and mentor.
Thank you to my committee members Miles Silman, Kathy Kron and Ron Dimock who wholeheartedly agreed to serve even though I am sure they were unaware of the length of this commitment (longer than some professors’ tenure at WFU and some marriages).
Special thanks to John Baxley who has had to come out of retirement to fulfill his duties as Chairperson of my examining committee. Thank you also to Mike Sprague, Spencer
Bissett and Scott Graham who assisted in many aspects of both lab and field data collection (lots of time spent on the beach). To the many undergraduates that have come and gone in the Smith ecophysiology lab over the years and who have taken many measurements for me, thank you. Thank you to Allison Snow whose data appears in
Chapter V.
Thank you to my family who has gone above and beyond in their support of me –
Cheryl Hancock (my wife), Hollie Lynn (daughter) and Anna Grace (daughter). There were many, many days, nights and weekends that Dad was away. May it be worth the pain and suffering. Finally, thank you to my mom and dad who have seen me grow and develop from Kindergarten until the present. I hope you are proud.
ii TABLE OF CONTENTS
ACKNOWLEDGEMENTS…………………………………………………………….....ii
LIST OF TABLES………………………………………………………………………...v
LIST OF FIGURES…………………………………………………………………...... vi
ABSTRACT……………………………………………………………………………….x
Chapter
I. INTRODUCTION
Study Site..………..……………………………………………………….2
Species………...…………………………………………………………..3
Literature Cited……………………………………………………………4
II. BARRIER ISLANDS, RELEVENT RESEARCH AND SPECIES SPECIFICS
The Dynamic Nature of Barrier Islands………………………………….13
A Review of Relevant Beach Plant Ecology Research………...…...……19
A Review of Relevant Physiological Plant Ecology Research….....…….24
Species Specifics…………………………………………………………26
Literature Cited…………………………………………………………..34
III. LEAF FORM AND FUNCTION: TESTING A MODEL
Introduction………………………………………………………………47
Materials and Methods………………………………………….………..50
Results………………………………………...………………………….53
Discussion…………………………………………………………..……57
Literature Cited…………………………………………………..…..…..64
IV. IMPORTANCE OF AND RESPONSE TO WATER STRESS IN BARRIER
iii ISLAND BEACH PLANT SPECIES
Introduction………………………………………………………………81
Materials and Methods……………………………...………..…………..84
Results……………………………………………..…………….……….87
Discussion……………………………………………..…………………97
Literature Cited……………………………………………..…..………106
V. USE OF PHOTOSYNTHETIC CARBON GAIN AS A COMMON
CURRENCY: MODELING RESPONSE OF FOUR PLANT SPECIES TO THE
PRESENT DAY BARRIER ISLAND BEACH ENVIRONMENT
Introduction…………………………………………………………..…123
Materials and Methods……………………………………….…………125
Results…………………………………………………………...... ……129
Discussion………………………………………………………………134
Literature Cited……………………………..…………..…………..…..141
VI. CONCLUSIONS AND PREDICTIONS FOR THE FUTURE OF FOUR
BARRIER ISLAND BEACH PLANT SPECIES IN RESPECT TO CLIMATE
CHANGE………………………………….……………………...... 163
CURRICULUM VITAE…………..……………………………………………172
iv LIST OF TABLES
Table I-1. Amaranthus pumilus, Cakile edentula, Hydrocotyle bonariensis
and Iva imbricata representing different plant functional groups………………...7
Table IV-1. Average daily distribution and total monthly rainfall (cm) on
Topsail Island, NC 1 July 2002 through 30 June 2003…………………………113
Table IV-2. Soil water content (%) of 100 g substrate samples taken at
different depths from Topsail Island, NC in the spring and summer
of 2004……………...... 114
-2 -1 Table V-1. Total assimilation (mol CO2 m day ) for Amarnathu pumilus,
Cakile edentula, Hydrocotyle bonariensis and Iva imbricata during
representative days from June 2002 until May 2003…………………………..148
-2 -1 Table V-2. Total monthly assimilation (mol CO2 m month ) for Amaranthus
pumilus, Cakile edentula, Hydrocotyle bonariensis and Iva imbricata
From June 2002 until May 2003……………………………………………….149
Table V-3. Best-fit equations for the photosynthetic light response of
Amaranthus pumilus, Cakile edentula, Hydrocotyle bonariensis and
Iva imbricata……………………………………………………………………150
v LIST OF FIGURES
Figure I-1. Global distribution of major coastal barrier island ecosystems………………8
Figure I-2. Formerly 3rd row home now within the intertidal zone
of North Topsail Beach, North Carolina…………………………………………..9
Figure I-3. Specific study site located on the southwestern end of Topsail
Island, North Carolina……………………………………………………………10
Figure I-4. Habitats located within the barrier island beach environment on
the southwestern end of Topsail Island, North Carolina……………………..…..11
Figure I-5. Amaranthus pumilus, Cakile edentula, Hydrocoytle bonariensis
and Iva imbricata representing different plant functional groups
living in the barrier island beach environment on the southwestern end
of Topsail Island, North Carolina…………..……………………………………12
Figure III-1. Photosynthetically Active Radiation (PAR) measurements taken
on representative days during 2002 and 2003…………………………………...70
Figure III-2. Average adaxial and abaxial stomatal frequencies of four species
of North Carolina (USA) barrier island beach plants………………………..…..71
Figure III-3. Transverse leaf cross sections of (A) Amaranthus pumilus, (B)
Cakile edentula, (C) Hydrocotyle bonariensis and (D) Iva imbricata………...... 72
Figure III-4. Schematic cross section of an Amaranthus pumilus leaf………………….73
Figure III-5. Schematic cross section of a Cakile edentula leaf………………………...74
Figure III-6. Schematic cross section of a Hydrocotyle bonariensis leaf……………….75
Figure III-7. Schematic cross section of an Iva imbricata leaf………………………….76
Figure III-8. Photosynthetic light response of Amaranthus pumilus leaves
vi
illuminated on the adaxial and abaxial leaf surfaces…………………………….77
Figure III-9. Photosynthetic light response of Cakile edentula leaves
illuminated on the adaxial and abaxial leaf surfaces…………………………….78
Figure III-10. Photosynthetic light response of Hydrocotyle bonariensis
leaves illuminated on the adaxial and abaxial leaf surfaces………………….….79
Figure III-11. Photosynthetic light response of Iva imbricata leaves
illuminated on the adaxial and abaxial leaf surfaces…………………………….80
Figure IV-1. Daily rainfall totals on Topsail Island, NC from 1 July 2002
until 30 June 2003………………………………………………………………115
Figure IV-2. Photosynthetically Active Radiation (PAR) measurements taken
on representative days during 2002 and 2003…………………………..………116
Figure IV-3. Diagramatic representation of Amaranthus pumilus, Cakile
edentula, Iva imbricata, and Hydrocotyle bonariensis life-history
traits on Topsail Island, NC…………………………………………………….117
Figure IV-4. Diurnal xylem water potential (Ψ) measurements taken on
representative days during 2002-2003……………………………………….…118
Figure IV-5. Diurnal assimilation rates (A) taken on representative days
during 2002-2003……………………………………………………………….119
Figure IV-6. Diurnal stomatal conductance rates (g) taken on representative
days during 2002-2003…………………………………………………………120
Figure IV-7. Diurnal transpiration rates (E) taken on representative days
During 2002-2003………………………………………………………………121
Figure IV-8. Diurnal xylem water potential measurements (Ψ), assimilation
vii
rates (A), conductance rates (g) and transpiration rates (E) taken on
21 Jun 2002…………………………………………………………………..…122
Figure V-1. PAR measurements taken on representative days during 2002
and 2003……………………………………………………………………...…151
Figure V-2a. Diurnal assimilation rates (A) taken once per month from
June 2002 until September 2002……………………………………………..…152
Figure V-2b. Diurnal assimilation rates (A) taken once per month from
October 2002 until January 2003……………………………………………….153
Figure V-2c. Diurnal assimilation rates (A) taken once per month from
February 2003 until May 2003……………………………………………...….154
Figure V-3. Photosynthetic light response of Amaranthus pumilus, Cakile
edentula, Hydrocotyle bonariensis and Iva imbricata measured on
7 July 2002…………………………………………………………………...…155
Figure V-4. Predicted (A) and actual (B) photosynthetic carbon gain (PCG)
for Amaranthus pumilus, Cakile edentula, Hydrocotyle bonariensis
and Iva imbricata……………………………………………………….………156
Figure V-5. Schematic diagram of the three Amaranthus pumilus
transplantation sites on Topsail Island, NC……………………………..….…..157
Figure V-6. Diurnal photosynthesis for representative Amaranthus pumilus
Plants at each of the transplantation sites as well as individuals found
naturally growing in the driftline and foredune habitats………………………..158
Figure V-7. Conceptual model of how photosynthetic carbon gain (PCG)
Thresholds could relate to life-history stages in Amaranthus pumilus...... 159
viii
Figure V-8. Photosynthetic light response of Amaranthus pumilus plants
Both inundated and non-inundated with saltwater during a 9 July 2004
overwash event on Topsail Island, NC (A.G. Snow, unpublished data)…….....160
Figure V-9. Conceptual model of barrier island beach abiotic stresses,
species response and resultant photosynthetic carbon gain (PCG)……………..161
Figure V-10. Idealized relationship between abiotic stresses, plant response,
photosynthetic carbon gain (PCG), allocation patterns and fitness
in the barrier island beach environment………………………………………..162
Figure VI-1. Southwestern end of Topsail Island before (6 August 2001) and after (6
October 2001) a storm overwash event……………………………………...…171
ix ABSTRACT
Hancock, Thomas, E.
ECOPHYSIOLOGY OF BARRIER ISLAND BEACH PLANTS: RESPONSES IN FORM AND FUNCTION TO DAILY, SEASONAL AND EPISODIC STRESSES
Dissertation under the direction of William K. Smith, Ph.D., Charles H. Babcock Professor of Botany
Barrier islands (BIs) are transient, highly dynamic geological structures of fairly
recent origin found along most continental shorelines. In particular, eighty-five percent
of the East and Gulf Coasts of the United States are fronted by BIs. Within this
environment, the BI beach is considered physically controlled due to the harsh abiotic
factors that predominate. The small suite of plant species that survive in this habitat have
been the subject of numerous ecological studies for greater than one-hundred years. This
research has provided a general understanding of how BI beach plants and their
environment interact and affect one another. Unfortunately, research on the
physiological ecology of BI beach plants is essentially nonexistent, with the exception of
several West Coast (USA) studies, and therefore a detailed understanding of the
physiological processes involved in plant response to stress is lacking. The most general objective of this dissertation is to incorporate the tools of physiological ecology into an ecological study that investigates the response of four plant species representing different functional groups to daily, seasonal and episodic stresses present on Topsail Island, North
Carolina (USA).
x Leaf stomatal frequency measurements, microscopic examination of internal leaf
anatomy and photosynthetic light response measurements of Amaranthus pumilus, Cakile
edentula, Hydrocotyle bonariensis and Iva imbricata were made in an effort to test
predictions of a leaf form and function model proposed by Smith et al. (1997).
Amaranthus pumilus, a C4 summer annual, had more stomata on the adaxial than abaxial
leaf surface, typical Kranz anatomy, and higher adaxial photosynthetic light response.
Cakile edentula, a C3 cool weather annual, had slightly more stomata on the adaxial leaf
surface, unifacial leaf anatomy and equal adaxial and abaxial photosynthetic light
response. Hydrocotyle bonariensis, a C3 perennial that grows by asexual rhizomes, had
equal numbers of stomata on both leaf surfaces, bifacial leaf anatomy and equal adaxial
and abaxial photosynthetic light response. Iva imbricata, a C3 woody perennial, had
equal numbers of stomata on both leaf surfaces, unifacial leaf anatomy and equal adaxial
and abaxial photosynthetic light response. These results generally fit model predictions for a stressful environment.
In a second study, micrometeorological measurements were taken and soil water content determined in an effort to assess water availability in the BI beach environment.
Additionally, plant strategies for mediating water stress were addressed via life-history trait determination, xylem water potential and gas exchange measurements. Moderate to high levels of rainfall occurred February through September, with forty percent of the yearly total associated with three storm systems (March, May and August). Soil water content was approximately three percent which is similar to values reported for several previous BI studies. Amaranthus pumilus had the shortest growing season (seven months), some of the highest assimilation rates and appeared to mediate transpiration and
xi xylem water potential via stomatal control. Cakile edentula was absent during the hottest
months of the year when vapor pressure deficits would have been greatest (late July
through late October). Cakile edentula had moderate to high assimilation rates, some of
the highest stomatal conductance rates and lowest xylem water potential measurements.
Hydrocotyle bonariensis exhibited the longest growing season (ten months), lowest assimilation rates and maintained an almost constant, high xylem water potential due to
rhizomes that accessed water from slacks located inland of the foredunes. Iva imbricata had a nine month growing season, moderate assimilation and transpiration rates as well as moderate xylem water potential values. Based on these findings, A. pumilus, H. bonariensis and I. imbricata could be considered to employ tolerance strategies with C. edentula employing an avoidance strategy.
The importance of photosynthetic carbon gain (PCG) as a common currency was addressed in a third study by modeling the response of A. pumilus, C. edentula, H. bonariensis and I. imbricata to the present day BI beach environment.
Micrometeorological, gas exchange and photosynthetic light response measurements as well as a transplantation experiment were conducted to estimate potential and realized
-2 PCG for each species. The realized yearly PCG was 63.14 mol CO2 m , 69.91 mol CO2
-2 -2 -2 m , 59.10 mol CO2 m and 80.16 mol CO2 m for A. pumilus, C. edentula, H.
bonariensis and I. imbricata, respectively. A PCG model based upon PAR measurements and the photosynthetic light response of each species suggested that there
were several environmental factors responsible for the difference in realized and potential
PCG. The response of each species to environmental stresses (including the genetic potential to respond to these stresses) can account for species differences in both potential
xii and realized PCG. A yearly PCG threshold may exist, as well as numerous life-stage
PCG thresholds, that must be met in order for plants to survive and produce viable offspring. Each species in this study can acquire these thresholds via a unique combination of life-history, anatomical and physiological attributes.
The final chapter of this dissertation explored predictions for the future of A. pumilus, C. edentula, H. bonariensis and I. imbricata in the face of climate change.
Many studies have indicated that in addition to a continuing (and possibly accelerated) rise in sea level, the intensity and frequency of extreme episodic storm events are likely to increase. These pressures when added to current and future habitat loss due to development and hardening of the shoreline will certainly result in a very different BI beach landscape than is seen today. Shorelines are predicted to retreat a few kilometers to tens of kilometers inland depending upon geographic location. How humans respond to these changes will determine the future of many BI beach plant species. Of the four species addressed in this study, A. pumilus is likely to be most negatively affected.
Amaranthus pumilus was listed as federally threatened in 1993 due to habitat loss.
Studies have shown that A. pumilus requires areas of suitable habitat that include accreting ends of BIs that do not contain hardened structures. These habitats are likely to become less common except in areas that are preserved or properly managed as dynamic landscapes. The Coastal Barrier Island Network is a recently funded (National Science
Foundation) diverse group of biologists, geologists, engineers, economists and sociologists that have begun to work toward a national policy that promotes sustainable preservation, conservation and development of BI ecosystems within the natural limits imposed by this highly dynamic environment.
xiii CHAPTER I
INTRODUCTION
Barrier islands are relatively young, dynamic, and transient geological features found along most continental shorelines (Figure I-1). The barrier island (BI) beach environment is physically controlled by daily, seasonal and episodic stresses whose intensities vary widely. These stresses are thought to have important implications for plant physiology, growth, reproduction and survival, ultimately dictating plant distribution patterns. The most general objective of this dissertation is to incorporate the tools of physiological ecology into an ecological study that investigates the response of
four plant species representing different functional groups (as defined by Shao et al.
1996, Crawford 2008) to daily, seasonal and episodic stresses present on a North
Carolina BI beach.
Chapter I provides an introduction to the study site, study species and dissertation objective. Chapter II reviews the dynamic nature of BIs, relevant ecological and ecophysiological studies and specifics of the study species. Leaf form and function in respect to a model proposed by Smith et al. (1997) is examined in Chapter III. Chapter
IV investigates water availability and adaptations to plant water stress in the BI beach environment. Photosynthetic carbon gain (PCG) as a common currency is explored in
Chapter V along with qualitative modeling of abiotic stressors, plant response and species fitness in the BI beach environment. Chapter VI focuses on predictions for the future of these plants in respect to global climate change.
1 Study Site
Topsail Island, North Carolina (USA) served as the study location for all
investigations in the following chapters. Topsail Island is a low topographic relief, 42 km
long barrier island that varies in width from 150 to 500 m located approximately 40 km
northeast of Wilmington, North Carolina (Stallman 2004). The island is bounded on its
northeastern end by New River Inlet and by New Topsail Inlet on its southwestern end.
It is extensively developed with single family homes and cottages along its length
(Frankenberg 1997). North Topsail Island has been designated as one of the highest risk real estate development zones in the United States due to erosion caused by the southwestern migration of New River Inlet as well as overwash from extreme episodic storm events (Pilkey et al. 1998, Pilkey and Pilkey-Javis 2007). Many formerly 2nd and
3rd row homes are now within the intertidal zone (Figure I-2).
Since 1900, North Carolina has averaged one hurricane strike every four years, including two exceptionally intense periods of activity during 1953-1960 and 1993-1999
(Barnes 2001). Topsail Island experienced four devastating hurricanes during the mid to
late 1990’s with Hurricane Bertha (1996) flooding over 1/3 of the island land area and
destroying most of the structures on the northeast end of the island, Hurricane Fran
(1996) destroying nearly all 1st row homes along the entire length of the island and
Hurricane Bonnie (1998) and Tropical Storm Dennis (1999) damaging many newly
repaired structures (Barnes 2001).
The specific study site was located on the southwestern end of the island (34o 20’
50” N, 77o 39’ 5” W) adjacent to New Topsail Inlet (Figure I-3). Due to migration of the
inlet to the southwest at an average rate of 35 m per year, an extensive beach
2 environment extends approximately 1-2 km from the last beach home to the inlet. Within
this beach environment a number of habitats can be defined and within each habitat a
number of species can be found (Figure I-4).
Species
Amarnathus pumilus Rafinesque, Cakile edentula (Bigelow) Hooker, Hydrocotyle bonariensis Lamarck and Iva imbricata Lamarck were choosen for the current study as representative of different functional plant groups (Table I-1, Figure I-5) that occupy the same BI beach environment. The following chapters will detail investigations that compare and contrast the structural, physiological, and ecological aspects of each species in an attempt to evaluate mechanisms enabling their growth, reproduction, and survival within their respective microhabitats in the BI beach community. Speculation about future impacts of current scenarios for global climate change is also presented in Chapter
VI.
Amaranthus pumilus
Amaranthus pumilus is a pioneer C4 annual species that inhabits the driftline and
foredune area of the BI beach (Weakley and Bucher 1992). Thus, this species has a
distinct photosynthetic physiology that differs from the other three study species (all C3 plants). The whole-plant architecture consists of a prostrate growth form, succulent leaves and pink to reddish stems. Acting as a low-lying sand collector, A. pumilus creates microtopographic mounds as the growing season progresses. These plants often become
30 cm in diameter, occasionally producing crowns with nearly 100 cm diameter ground cover (Weakley and Bucher 1992). As a result of population decline due to habitat loss,
3 A. pumilus was listed as federally threatened in 1993 (United States Fish and Wildlife
Service 1993).
Cakile edentula
Cakile edentula is a pioneer C3 annual species that has an upright growth form
and succulent leaves (Radford et al. 1968). The plant is common within its range
(Barbour and Rodman 1970) and unlike A. pumilus, C. edentula can persist into a second
growing season in moderate climates (Barbour and Rodman 1970, Boyd and Barbour
1993, Cody and Cody 2004).
Hydrocotyle bonariensis
Hydrocotyle bonariensis is a C3 perennial species whose range includes the Gulf and East Coasts of the United States as well as locations in South America (Radford et al.
1968, Evans 1992). Seeds only germinate in swales located landward of the primary dune on BI beaches. Plants can grow seaward into the foredune via rhizomes (Evans
1992). Leaves are peltate, vary in width from 4 to 12 cm and senesce in winter with the rhizomes persisting underground until the next growing season (Radford et al. 1968).
Iva imbricata
Iva imbricata is a woody C3 shrub with succulent leaves found along the coasts of
southern Virginia to the Florida Keys, Gulf Coast of the United States and on beaches of
Caribbean islands (Jackson 1960). The plant can grow to heights of 1 m and widths of
3 m (Radford et al. 1968). As a seedling, I. imbricata coinhabits the driftline with A. pumilus and C. edentula.
Literature Cited
Barbour, M.G. and J.E. Rodman. 1970. Saga of the west coast sea-rockets: Cakile edentula ssp. californica and C. maritima. Rhodora. 72:370-386.
4
Barnes, J. 2001. North Carolina’s Hurricane History (3rd edition). The University of North Carolina Press, Chapel Hill, NC (USA).
Boyd, R.S. and M.G. Barbour. 1993. Replacement of Cakile edentula by C. maritima in the strand habitat of California. American Midland Naturalist. 130:209-228.
Cody, M.L. and T.W.D. Cody. 2004. Morphology and spatial distribution of alien searockets (Cakile spp.) on South Australian and Western Canadian beaches. Australian Journal of Botany. 52:175-183.
Crawford, R.M.M. 2008. Plants at the Margin. Cambridge University Press, Cambridge (GRB).
Evans, J.P. 1992. Seedling establishment and genet recruitment in a population of a clonal dune perennial. Barrier Island Ecolgoy of the Mid-Atlantic Coast: a Symposium. Technical Report NPS/SERCAHA/NRTR-93/04.
Frankenberg, D. 1997. The Nature of North Carolina’s Southern Coast. The University of North Carolina Press, Chapel Hill, NC (USA).
Jackson, R.C. 1960. A revision of the genus Iva L. University of Kansas Science Bulletin. 41:793-896.
Pilkey, O.H. 2003. A Celebration of the World’s Barrier Islands. Columbia University Press, New York, NY (USA).
Pilkey, O.H., W.J. Neal, S.R. Riggs, C.A. Welsh, D.M. Bush, D.F. Pilkey, J. Bullock and B.A. Cowan. 1998. The North Carolina Shore and its Barrier Islands: Restless Ribbons of Sand. Duke University Press, Durham, NC (USA).
Pilkey, O.H. and L. Pilkey-Jarvis. 2007. Useless Arithmetic: Why Environmental Scientists Can’t Predict the Future. Columbia University Press, New York, NY (USA).
Radford, A.E., H.E. Ahles and C.R. Bell. 1968. Manual of the Vascular Flora of the Carolinas. The University of North Carolina Press. Chapel Hill, NC (USA).
Shao, G., H.H. Shugart and B.P. Hayden. 1996. Functional classification of coastal barrier island vegetation. Journal of Vegetation Science. 7:391-396.
Smith, W.K., T.C. Vogelmann, E.H. DeLucia, D.T. Bell and K.A. Shepherd. 1997. Leaf form and photosynthesis. Bioscience. 47:785-793.
Stallman, D.A. 2004. Echoes of Topsail. Carlisle Printing, Sugarcreek, OH (USA).
5 United States Fish and Wildlife Service. 1993. Endangered and threatened wildlife and plants: Amaranthus pumilus (seabeach amaranth) determined to be threatened. Federal Register 58(65):18035-18041.
Weakley, A.S. and M.A. Bucher. 1992. Status survey of seabeach amaranth (Amaranthus pumilus Rafinesque) in North and South Carolina. Report to the North Carolina Plant Conservation Program and Endangered Species Field Offfice, North Carolina (USA).
6 Table I-1. Amaranthus pumilus, Cakile edentula, Hydrocotle bonariensis and Iva imbricata representing different plant functional groups.
Species Growth Leaf Orientation Leaf Form Photosynthetic Reproduction Length of Form and thickness Pathway Growing Season o Amaranthus herbaceous, 90 angle from spatulate, C4 seeds 6-7 months pumilus prostrate incident sunlight 3 mm ~ 3 mm long
o Cakile herbaceous, 45 angle from sinuately lobed, C3 seeds 9 months edentula erect incident sunlight often crenate, ~ 4-6 mm long 4 mm
Hydrocotyle herbaceous, leaf angle and elliptate, C3 seeds ~ 1-2 mm 10 months bonariensis clonal azimuth can change 2 mm long, clonal daily and growth seasonally
o Iva imbricata deciduous, varies from 45 to peltate, C3 seeds 9 months shrub 90o angle from 4 mm ~ 4-5 mm long incident sunlight
7
Figure I-1. Global distribution of major coastal barrier island ecosystems (indicated by dots). Arrows call attention to delta barrier islands. Taken from Pilkey (2003).
8
Figure I-2. Formerly 3rd row home now within the intertidal zone of North Topsail Beach, North Carolina. (Photographed by William K. Smith)
9
N WE North Carolina
S
study site
Figure I-3. Specific study site located on the southwestern end of Topsail Island, North Carolina.
10
1o dune
foredunes ocean beach face driftline swale
A. pumilus, C. edentula
I. imbricata
H. bonariensis
Figure I-4. Habitats located within the barrier island beach environment on the southwestern end of Topsail Island, North Carolina. The general positions of Amaranthus pumilus, Cakile edentula, Hydrocotyle bonariensis and Iva imbricata are indicated.
11
Amaranthus pumilus Cakile edentula
Iva imbricata Hydrocotyle bonariensis
Figure I-5. Amaranthus pumilus, Cakile edentula, Hydrocoytle bonariensis and Iva imbricata representing different plant functional groups living in the barrier island beach environment on the southwestern end of Topsail Island, North Carolina.
12 CHAPTER II
BARRIER ISLANDS, RELEVENT RESEARCH AND SPECIES SPECIFICS
The Dynamic Nature of Barrier Islands
Barrier islands are found on approximately 15% of the world’s shorelines with some of the most extensive chains located along the Atlantic and Gulf Coasts of North
America (Ehrenfeld 1990, Figure I-1). In particular, 85% of the East and Gulf Coasts of the United States contain BIs (Snyder and Boss 2002, Stive and Hammer-Klose 2004,
Adger et al. 2005). Barrier islands occur in greatest abundance along microtidal and mesotidal coasts that exhibit low-relief coastal plains and wide continental shelves that are comprised of abundant sediments readily reworked by wave action (Glaeser 1978,
Ehrenfeld 1990, Hayden et al. 1991, Pilkey et al. 1998). In general, BI formation is dependent upon a dynamic equilibrium encompassing sea level rise, wave energy and sediment supply (Dolan et al. 1980, Hayden et al. 1991).
Paleogeology
During the Wisconsinan glaciation maximum which occurred around 18,000 years before present (ybp), sea level was approximately 300 feet lower than today
(Frankenburg 1997). As climate warmed and glaciers melted, a period called the
Holocene Transgression, sea level rose at a rate of 10 mm/year (Frankenburg 1995,
Pikley et al. 1998). This rate is thought to have been too rapid for BI formation (Dolan et al. 1980, Alexander and Lazell 2000, NOAA Coastal Services Center). When sea level rise slowed to about 2-3 mm/year, a relative equilibrium with sediment accumulation was
13 reached (Dolan et al. 1980, Hayden et al. 1991). It was during this time, approximately
5,000 – 7,000 ybp, that East Coast (USA) BIs began to form (Dolan et al. 1980,
Ehrenfeld 1990, Frankenberg 1995, Pilkey et al. 1998, NOAA Coastal Services Center).
Hydrogeological Theories of Barrier Island Geomorphology
Three principle theories of BI formation have been proposed (Schwartz 1971).
DeBeaumont (1845) suggested that near-shore ocean floor sediment is displaced by an
approaching wave. The sediment is then picked-up and transported until the wave
breaks, losing much of its energy. Subsequently, the sediment settles forming an offshore
bar. Over time, this offshore bar can build to such an extent that it emerges above the
water’s surface and forms a barrier island. Johnson, in his 1919 classic text on BIs,
supported DeBeaumont’s emergent bar theory of BI formation. More recently, Otvos
(1970) embraced the same theory citing the United States’ Gulf Coast BIs as examples.
Hoyt (1967) developed the dune ridge submergence theory suggesting that BIs
are formed when sea level rise causes the formation of a lagoon between coastal dune
ridges and the remaining mainland. The width of the island depends upon sand accretion
prior to or during submergence. The length of the island depends upon the continuity of
the dune ridge. Inlets are formed in areas of low elevation. The sea islands of South
Carolina and Georgia have been suggested as examples of BIs formed via this
mechanism (Schwartz 1971, NOAA Coastal Services Center).
Working along lake shores, Gilbert (1885) first proposed the breached spit theory
that supposes BIs are created from sediment transported by longshore currents. Spits that
form from the accretion of this sediment can be breached during storms, thus forming
BIs. Fisher (1968) was the first to apply this idea to marine coastlines. As explained by
14 Pilkey et al. (1998), when see level began to rise, water flooded river valleys changing a
formerly straight shoreline into a sinuous one. The formation of BIs is a mechanism that
attempts to straighten the shoreline. Waves attack protruding headlands forming spits,
these spits are later breached by storms and form inlets, thus defining the island. Most of
the BIs found in Virginia and North Carolina are thought to have formed in this manner
(Pilkey et al. 1998). In a review of the evidence for all three principle theories of BI formation, Schwartz (1971) concluded that each was viable and applicable in different geographic locations.
Depending upon sediment supply, rate of sea level rise and hydrodynamic factors,
BIs accrete and advance seaward, erode and retreat landward, or stabilize (Hoyt 1967).
Due to the repeated forming and melting of continental ice sheets, there have been at least
six discernable sequences of BI formation within the geologic past (Hoyt and Hails
1967). Sea level, however, has been rising at a moderate rate for the past 5,000 – 7,000
years resulting in landward migration and erosion of approximately 85% of the shoreline
of the United States (Pilkey et al. 1998, Pilkey and Pilkey-Javis 2007). According to the
4th Assessment Report of the Intergovernmental Panel on Climate Change (IPCC), global
average sea level is currently rising 3.1 mm/year (IPCC 2007). Storms that result in
landward transportation of sand via overwash are the main mechanism of BI migration
(Godfrey 1976, Frankenberg 1997). For example, a 1971 storm that occurred at Cape
Hatteras, North Carolina removed a large portion of the beach overnight, depositing the
majority of sand in overwash fans that extended into the marsh behind the island (Pilkey
et al. 1998 and Pilkey-Javis 2007).
Inlets
15 Inlets spatially define the boundaries of most BIs and are notoriously unstable, resulting in BI migration up or down a coastline depending upon local conditions (Pilkey et al. 1998). For example, twenty-four inlets have existed at one time or another along the North Carolina Outer Banks since 1585. Five of these inlets are currently open
(Frankenberg 1995). The instability of these BIs has resulted in the region being aptly named “The Graveyard of the Atlantic” due to the hundreds of ships that have run aground and sunk (Stick 1952, Stick 1958). New Topsail Inlet, North Carolina has been
migrating 30 – 40 m to the southwest per year since at least the early 1930’s (Pilkey et al.
1998, Stallman 2004). Two recent examples of inlet closure include Mad Inlet between
Bird Island and Sunset Beach, North Carolina and Old Topsail Inlet between Lea and
Hutaff Islands, North Carolina (personal observation). New inlets can also form during storms. Three inlets, for example, were opened on Topsail Island during hurricane Fran in 1996 (Barnes 2001).
Beach stress
Historically, ecologists have recognized the dynamic nature of the BI beach environment, describing it as being physically controlled (Oosting 1954, van der Valk
1974a, Godfrey 1976). Abiotic factors such as high substrate surface temperatures, low water-holding capacity, sand movement, salt aerosols, high irradiance levels and storms that result in overwash have been implicated in controlling plant distribution patterns (see
Ehrenfeld 1990 for review). These factors occur over a continuous timeframe, but for ease of discussion can be categorized into daily, seasonal and episodic stresses.
Daily and seasonal stresses
16 Daily stresses present on a North Carolina BI beach include substrate surface temperatures as high as 52oC (Oosting and Billings 1942), rapid vertical movement of rainfall through the substrate resulting in low moisture levels (Au 1974), burial by sand
(Martinez and Moreno-Casasola 1993), salt deposition on leaves (Boyce 1954) and irradiance values of 2000 μmol of photons m-2 s-1 for extended periods of time (personal observation). An important seasonal stress is late fall to early spring storms that move large quantities of sand to the offshore sandbar, essentially defining the line of vegetation for the following growing season (Rogers and Nash 2003, Miyanishi and Johnson 2007).
In addition to the mechanical destruction caused by these seasonal overwash events, salt- water inundation has been found to have many deleterious effects on plants often resulting in death of annuals and reduction of perennial biomass (DeJong 1978b, Schat and Scholten 1986, Guy et al. 1989, Ungar 1991, Alpha et al. 1996, Martinez et al. 2002).
In contrast to these traditional studies, however, Greaver and Sternberg (2006) found that foredune plants living on their Floridian and Bahamian study sites were able to utilized ocean water as a water source.
Episodic stress
Episodic stresses such as hurricanes, which have been termed Extreme Episodic
Storm Events (EESE) by Feagin et al. (2009), are considered the dominant force influencing species composition in some coastal systems (Turner et al. 1997, Miyanishi and Johnson 2007, CBIN). Gutshick and BassiriRad (2003) expanded this idea stating that extreme events are the driving force in trait selection of most plants. Although
EESE, and to some extend seasonal stresses, have a disproportionate affect on the BI
17 environment (Pilkey and Pilkey-Javis 2007), their impact is influenced by daily abiotic
environmental gradients (Synder and Boss 2002, Stallings and Parker 2003).
Climate change impacts
All of the stresses mentioned previously, but especially those that are seasonal
and episodic, could be exacerbated by future climate change in which storm intensity and
frequency are predicted to increase (Goldenberg et al. 2001, Thompson et al. 2001,
Hayden and Hayden 2003, Holgate and Woodworth 2004, Pilkey and Cooper 2004,
Zhang et al. 2004, IPCC 2007, Elsner et al. 2008, Schlacher et al. 2008, Mann et al.
2009). Sea-level rise will most likely intensify the effect of storms on the BI beach
environment (Pilkey and Pilkey-Javis 2007), with particularly dire implications for the
North Carolina coast due to the large area of land that is within one meter of current
mean sea-level (Nash 2008). In a long-term study conducted on Core Banks North
Carolina, Riggs and Ames (2006) found that although there was only small-scale
shoreline recession over the forty-one year data set, storm events produced extremely
large-scale changes. The authors stated that if given enough time, barrier islands tend to
recover and approach their pre-storm location but this rarely occurs before another storm
makes landfall.
Climate change could affect organisms world-wide, indeed in a review by Cleland
et al. (2007) numerous plant studies were cited that found correlations between earlier
spring flowering and rising temperatures. Pike and Stiner (2007) discovered that rising
global temperatures were correlated with earlier nesting dates for loggerhead turtles along
Cape Canaveral National Seashore. Additional studies have revealed climate change effects on the ecology of many different species (reviewed in Parmesan 2006). Ongoing
18 climate change is considered to be a driving factor for ecosystems in the 21st century
(Jentsch et al. 2007), with loss of habitat and associated biota the most immediate threat to beaches (Schlacher et al. 2008). Crawford (2008) extends this sentiment by stating that an especially important danger to maritime vegetation will be the actions humans take to save their property from sea inundations.
A Review of Relevant Beach Plant Ecology Research
The study of dune plants has a long history dating back to the ecological work of
Cowles (1899) and Kearney (1900) and the anatomical/morphological studies of Chrysler
(1904), Kearney (1904) and Starr (1912), all undertaken within the United States. Early
work conducted on European dunes has been amply reviewed in the influential publications of Salisbury (1952) and later Ranwell (1972). More recent studies of
European dune plants accessed germination requirements (Pemadasa and Lovell 1975,
Ignaciuk and Lee 1980), mineral requirements (Pemadasa and Lovell 1974), plant distribution in relation to abiotic factors (Pemadasa et al. 1974) and demography
(Watkinson 1978, Watkinson and Harper 1978). In an attempt to remain as relevant as possible, given that Topsail Island, North Carolina (USA) is the study site for this
dissertation, the following discussion will focus on historical studies conducted within the
United States and in particular along the East Coast. The term “beach” includes all
habitats between the spring high tide line and the back of the primary dune.
East Coast (USA)
Cowles, in his 1899 study located along the dunes of Lake Michigan, emphasized
the dynamic nature of vegetation in relation to local geology. Studies on the importance
of physical factors as major controls in the dune environment were greatly expanded by
19 Oosting in a series of experiments undertaken on several barrier islands (BIs) located
near Beaufort, North Carolina (Oosting 1945, 1954, Oosting and Billings 1942). After
careful documentation and experimentation with many aspects of the physical
environment, Oosting concluded that salt spray was the main factor determining the
distribution of perennials on the BI beach. Wells (1939) came to a similar conclusion in
that salt spray was the limiting factor allowing Quercus virginiana Miller to become the
dominant species in the maritime forest found on Smith Island located at the mouth of the
Cape Fear River, North Carolina. Alternatively, van der Valk (1974a, 1975) stated that
sand movement was the main limiting factor to the distribution of annuals on the dunes in
Cape Hatteras National Seashore, North Carolina. He additionally documented macro
and microclimate aspects of the BI beach environment and developed a model of nutrient
cycling involving salt spray (1974b, 1977).
Boyce (1954) undertook an exhaustive study of the salt spray community found
on Smith Island. This research still serves as the basis for our understanding of salt spray
effects on plant morphology, physiology and ecology. In a later study, Art et al. (1974)
determined that the major nutrient input into the maritime forest of Fire Island, New York was via salt spray. Au (1974) published a monograph of the ecological processes on
Shackleford Bank, North Carolina in which he reported that substrate moisture levels
were low (3 – 4%), but remarkably consistent – a finding echoed by van der Valk
(1974b). In the same studies, Au made some of the earliest water potential measurements
for East Coast BI beach plants and concluded that water availability was not a limiting
factor for growth.
20 While studying the dune system on Cape Lookout National Seashore, Godfrey
(1976) concluded that the North Carolina Outer Banks were migrating landward, that
storms play a critical role in this migration and that overwash was the major mechanism
of movement. Hosier and Cleary have come to similar conclusions about BIs along
North Carolina’s southern coast (Hosier and Cleary 1977, Cleary and Hosier 1979).
The majority of BI plant ecology research has found that physical factors determine plant distribution patterns (see Ehrenfeld 1990 for review). There are, however, a handful of studies that indicate biological interactions are influential and therefore must be considered. Silander and Antonovics (1982) employed a perturbation approach on Core Banks, North Carolina, in which they removed dominant and subdominant species either singly or within groups and documented response of the remaining species. They were able to detect significant species interactions, concluding that these interactions are important in structuring the dune community. In a series of studies conducted on BIs in Georgia and Florida, Franks (2003a, 2003b, Franks and
Peterson 2003) documented significant nurse plant effects especially with increasing disturbance severity, concluding that facilitation is important in coastal dune succession.
In a number of studies conducted by North Carolina State University researchers, much of the growing knowledge about dune plant ecology was applied to dune stabilization (Woodhouse and Hanes 1966, Woodhouse et al. 1968, Woodhouse et al.
1976, Woodhouse 1978). The general findings of these studies were that perennial plants such as Ammophila breviligulata Fernald, Uniola paniculata Linnaeus and Panicum amarum Elliot could be successfully grown in greenhouses, transplanted into the dune environment and act as sand traps that build dunes. Watering during the first few weeks
21 after transplantation and fertilization four times per year were critical determinates of
seedling and plant survival. Recently, there has been renewed interest in using native
vegetation (Rogers and Nash 2003) and especially Quercus virginiana, to help stabilize
BIs (Feagin et al. 2009, CBIN).
Great Lakes (USA) and Canada
Keddy (1981, 1982) conducted a series of experiments on a beach in Nova Scotia using Cakile edentula (Bigelow) Hooker, a common C3 winter annual. In these
experiments, he was able to develop a model for C. edentula incorporating density-
dependent and density-independent environmental factors that accurately predicted
survivorship and reproduction along an environmental gradient. Working on the dune
system of Lake Huron, Zhang and Maun (1992) determined that sand burial increased
plant growth and reproductive output. Growth was the greatest in unwashed sand which
may suggest possible beneficial mycorrhizal interactions. Using similar study sites,
Payne and Maun (1984) determined that desiccation, insect damage, disease infection and
human trampling were major causes of C. edentula seedling death. Maun and Lapierre
(1986) reported a positive relationship between seed weight and depth of emergence for
several dune species.
Zhang and colleagues focused on the dimorphic nature of C. edentula seeds in
another set of studies also undertaken along the Lake Huron dunes. The authors found
that upper seeds were selected for dispersal while lower seeds remained on the parent
plant (Zhang 1994), seed mass and morphology could indirectly affect life history traits
(Zhang 1993) and several dune species including C. edentula have the ability to form a
persistent seed bank (Zhang and Maun 1994). Zhang (1996) expressed the need for
22 coastal dune studies to include experimental designs that test the importance of multiple
environmental factors on plant growth and survival.
West Coast (USA)
Barbour and Rodman (1970) chronicled the introduction and subsequent spread of
Cakile edentula and Cakile maritima Scopoli along the West Coast of the United States in a descriptive study that included details of the plants’ life-history traits. Barbour
(1970) added to this descriptive knowledge in a series of experiments that included both laboratory and field manipulations involving germination and growth response of C. maritima to temperature, light and salt spray. In an attempt to determine causative factors for zonation patterns, Barbour and DeJong (1977) discovered that, when tested separately, tolerance to salt spray and salt water inundation of nine California dune plants were strongly correlated with their distance from mean high tide. Three plants, however, did not fit predictions leading the authors to conclude that single-factor experimental designs were not sufficient to account for the distribution of all dune plants.
Improved salt trap designs based upon the earlier work of East Coast researchers
(Oosting 1945, 1954, Oosting and Billings 1942) allowed Barbour (1978) to develop comprehensive salt deposition maps that accurately accounted for the distribution of some dune plants. Building upon these studies, Boyd and Barbour (1986) determined that C. edentula var. lacustris (found along the Great Lakes) and C. edentula var. edentula (found along the East and West Coasts) had diverged physiologically over the past 9,000 years in part due to differences in salt tolerance. In several studies which focused on the historical and current distribution of C. edentula var. edentula and C. maritima in the dune habitat of California, Boyd and Barbour (1993) determined that the
23 ability of C. maritima to survive into a second and even third growing season may be the
main reason it replaced C. edentula var. edentula over a forty year period Preferential
seed predation by Peromyscus maniculatus, the common deer mouse, probably increased
the replacement rate (Boyd 1988, Boyd 1991).
A Review of Relevant Physiological Plant Ecology Research
The discipline of physiological plant ecology combines ecological and
physiological measurements in an attempt to explain plant distribution and abundance
(Billings 1985; Barbour et al. 1985; Lambers et al. 1998). According to Billings (1985), physiological ecology shared beginnings with the field of ecology and it was not until the development of transportable technologies allowing measurement of gas exchange and water balance that physiological ecology became distinct. Although the techniques of
physiological plant ecology have often been employed in many extreme environments
such as the desert and alpine timberline (Billings 1985), Barbour et al. (1985) found few
instances in which “modern approaches to gas exchange, water balance and plant
demography have been applied to beach taxa”. There has been little additional research
since the publication of that finding. The following paragraphs provide a short review of
the physiological plant ecology studies undertaken on coastal dunes.
DeJong completed a number of basic physiological ecology studies on the
northern California dunes in which he determined the photosynthetic maximum of
several species of plants in relation to light, temperature and CO2 concentrations inside the leaf (DeJong 1978a), compared photosynthetic response while growing in media of different salinities (DeJong 1978b) and characterized water balance in relation to the microclimate in which the plants grew (DeJong 1979). Taking measurements from sites
24 in both northern and southern California, Pearcy (1976) addressed the photosynthetic plasticity of Atriplex lentiformis in relation to thermal regimes, identifying ecotypic differences in the subpopulations found in each region. Mooney (1980) also found ecotypic variations when he conducted a similar study using Heliotropium curassavicum.
In another investigation, Mooney et al. (1983) characterized the physiological ecology of five herbaceous plants inhabiting the dunes of Point Reyes National Seashore in
California. Working at the same location, Pavlik (1983) not only documented the photosynthetic trends of Ammophila arenaria and Elymus mollis, but brought nitrogen use efficiency (NUE) and morphological traits into his discussion.
Using gas exchange and xylem water potential measurements, Ishikawa et al.
(1990) categorized plants living on Japanese dunes as heat-resistant, heat-enduring or heat-evading based upon their ecophysiological characteristics. The researchers continued their studies by examining plant distribution patterns in relation to plant soil water salinity tolerance (Ishikawa et al. 1991), site micrometeorological characteristics
(Ishikawa et al. 1995) and plant resistance to drought (Ishikawa et al. 1996). In a more recent study involving ten plant species inhabiting the Lake Erie sand dunes, Perumal and
Maun (2006) discovered that biomass, photosynthetic efficiency and chlorophyll-a fluorescence all increased in response to burial by sand.
In the only relevant physiological ecology study conducted on the East Coast
(USA), Dubois (1977) completed a very ambitious project in which she documented water use efficiency (WUE), NUE and photosynthetic rate in relation to temperature and xylem water potential of three C3 and five C4 species living on the Georgia dunes. She determined that C3 and C4 species had similar photosynthetic temperature response
25 curves, but that the C4 species had higher NUE and WUE which may be an important
adaptive advantage.
Species Specifics
Amaranthus pumilus
Amaranthus pumilus is a pioneering C4 annual species that inhabits the driftline and foredune area of the BI beach (Weakley and Bucher 1992). The plant has a prostrate growth form, succulent leaves and pink to reddish stems. Acting as a sand binder, A.
pumilus creates mounds as the growing season progresses. These plants often become 30
cm in diameter, occasionally producing growths 90 cm in diameter (Weakley and Bucher
1992).
Historically, A. pumilus was found from Nantucket, Massachusetts to Folly
Beach, South Carolina. By 1987, however, the plant was extirpated from nearly 75% of
its earlier range (Weaker and Bucher 1992). Due to population decline and continued
habitat loss from development, A. pumilus was listed as federally threatened in 1993
(United States Fish and Wildlife Service 1993). The current distribution of A. pumilus is
limited to North and South Carolina (United States Army Corps of Engineers 1992-1995,
Hancock and Hosier 2003) although several populations have reappeared in New York
(Clements and Mangels 1990, van Schoik and Antenen 1993) and Maryland (Ramsey et
al. 2000). Amaranthus pumilus population numbers have been documented to fluctuate
tremendously from year to year (Weakley and Bucher 1992, United States Corps of
Engineers 1992-1995, Strand 2002, Hancock and Hosier 2003).
Research involving Amaranthus pumilus is quite limited. The status survey conducted by Weakley and Bucher (1992) has served as the foundation for all subsequent
26 studies. Baskin and Baskin (1998) conducted an investigation to determine the
germination requirements of A. pumilus. They found that fresh seeds were
physiologically dormant, cold stratification broke this dormancy and light and high
temperatures (30oC) were required for germination. Norden et al. (2007) determined that
treatment of nonstratified A. pumilus seeds with solutions of potassium salt of gibberellin
A3 (K-GA3) removed physiological dormancy, reduced seed sensitivity to light and
broadened the temperature range for germination. Hamilton (2000) conducted a series of
propagation experiments which involved collecting A. pumilus plants growing at
Huntington Beach State Park, South Carolina and transplanting them to a greenhouse.
Plants were grown to reproductive maturity and seed was subsequently collected. The
seeds were germinated, allowed to grow for 4-6 weeks in the greenhouse and transplanted
to experimental test sites located adjacent to the original collection sites. Eighteen
percent of the transplanted plants produced seed the following fall.
Strand (2002) characterized the genetic structure of A. pumilus populations by
analyzing the amount and location of genetic variation at a variety of loci including
chloroplast DNA, introic regions of nuclear DNA and anonymous PCR-based markers
(RAPDS). He found no observable differences among individuals when comparing the
chloroplast DNA and introic regions of nuclear DNA data. The RAPDS data, however,
did reveal a pattern in which northern populations of A. pumilus were genetically distinct
from southern populations. Strand stated that it is possible that the Chesapeake Bay
provides a natural barrier to seed migration between these populations.
Other works of interest include a study in which Light Detection and Ranging
(LIDAR) and Geographic Information Systems (GIS) were used to determine and model
27 suitable habitat for A. pumilus (Sellars and Jolls 2007), an investigation of the chemical
components and composition of A. pumilus seed in respect to food value (Marcone 2000)
and a short note about Albugo bliti fungal infection on plants used in a restoration effort
in South Carolina after Hurricane Hugo (Keinath et al. 2003). Hancock and Hosier
(2003) completed an ecological study of A. pumilus in which they found no evidence for
biological control of population dynamics but determined that storm overwash was the
main factor limiting seedling survival and subsequent seed set for adult plants.
Additionally, they mentioned that the inability to emerge from depths greater than 1 cm
as well as a short growing season may be adaptive disadvantages when compared to BI
beach associates. Finally, Rosenfeld (2004) determined that distance from the ocean had
a significant effect on A. pumilus survivorship, size and reproduction. She attributed this
to gradients of physical factors such as soil salinity, salt spray and overwash rather than
biological interactions.
Cakile edentula
Cakile edentula is a pioneering C3 annual species that has an upright growth form and succulent leaves (Radford et al. 1968). The plant can reach heights of 60 cm with
widths of 70 cm (personal observation). Cakile edentula is common within its range
from southern Florida into Canada, along the West Coast of the United States and the shores of the Great Lakes (Barbour and Rodman 1970). Unlike A. pumilus, Cakile
edentula can persist into a second growing season in moderate climates such as the coasts
of California (Barbour and Rodman 1970, Boyd and Barbour 1993) and Australia (Cody
and Cody 2004). On the East Coast of the United States, C. edentula is often found in
association with A. pumilus and Iva imbricata growing just above the spring high tide
28 line (driftline) where it accumulates sand and begins the process of dune formation
(Colosi and McCormick 1978, Hancock and Hosier 2003, Rogers and Nash 2003).
Cakile edentula has been the subject of numerous ecological and ecophysiological studies (see Maun et al. 1990) as have been reviewed in Chapter I. In fact, the majority of experiments conducted on the dunes of the Great Lakes and West Coast of the United
States using ecophysiological techniques have involved C. edentula. There are, however, a few studies that have focused on other aspects of the biology of C. edentula or were undertaken in different locations.
Tyndall et al. (1986a) conducted an experiment at Currituck Beach, North
Carolina to ascertain why C. edentula was the dominant species in the beach habitat.
They discovered that C. edentula seeds were buoyant and that seedlings could emerge from greater depths than other beach or foredune associates; important factors given the high sand burial rate of the site. In a follow-up study meant to determine why C. edentula was preferentially found on beach versus foredune habitats, Tyndall et al.
(1986b) concluded that low soil water potential resulted in lower leaf water potentials and stomatal conductance values of C. edentula living in the foredune when compared with plants living on the beach.
In a laboratory germination study designed to mimic different microenvironmental conditions, Adair et al. (1990) found that increased soil moisture provided by wrack material (detritus) and deeper seed burial were responsible for increased germination rates of C. edentula. Gedge and Maun (1992) experimented with different levels of herbivory on C. edentula and discovered that plants were able to compensate for low to medium damage but that high levels of damage reduced growth
29 and reproductive output. The authors suggested that natural populations are able to avoid
high rates of destruction because herbivores have a difficult time locating plants.
Donohue conducted a series of studies focusing on dispersal, fitness, relatedness and selection in Cakile edentula growing along the shores of the Great Lakes. In one study, she determined that selection on dispersion patterns occurred through density effects rather than dispersal distance (Donohue 1997). Using the characteristic that fruits of C. edentula are divided into proximal segments that remain on the parent plant and distal segments that disperse (Maun et al. 1990), Donohue confirmed intuition by finding that proximal seeds had a greater probability of reproduction near the mother plant while distal seeds had a greater probability of reproduction at more distant sites. In a second study, she found that environmental factors strongly influenced the expression of plant traits which in turn influenced dispersal (Donohue 1998). In a third study, Donohue
(2003) investigated the influence of relatedness on C. edentula plants growing close to one another along the shores of Lake Michigan. She observed significant group selection on plant size when neighbors were siblings but not when they were unrelated and that individual and group selection operated in the same direction. In a final study, she noted that individual selection was detected at low density while group selection was detected at higher densities for C. edentula growing on the dunes of the Great Lakes
(Donohue 2004).
Dudley (1996a) conducted a study in which she raised C. edentula plants from a wet-site and a dry-site population in a common greenhouse environment. The dry-site population had significantly smaller leaf size and greater WUE than the wet-site. In a follow-on study, Dudley (1996b) used phenotypic selection analysis to test whether
30 smaller leaves and greater WUE were adaptive in drier environments. She found that in her experimental set-up, smaller leaves and greater WUE were selected for in the dry environment while neither were selected for in the wet environment. Additionally, WUE primarily affected plant fitness by increasing vegetative biomass. In a more recent experiment investigating kin recognition in plants, Dudley and File (2007) reported that allocation to the roots of C. edentula increased when groups of strangers shared a common pot but not when siblings shared a pot. They concluded that root interactions may provide cues for kin recognition.
Hydrocotyle bonariensis
Hydrocotyle bonariensis is a C3 perennial species whose seeds germinate in swales located landward of the primary dune on BI beaches (Evans 1992a). The plants can grow seaward into the foredune via rhizomes (Evans 1992a). Leaves are peltate, vary
in width from 4 to 12 cm and senesce in winter with the rhizomes persisting underground
until the next growing season (Radford et al. 1968). Hydrocotyle bonariensis is common
on the barrier islands of the southeastern United States and has been known to form
extensive populations where individual clones may cover 100 m2 and consist of greater
than 1500 ramets (Evans 1988).
Evans conducted a series of experiments in which he investigated the ability of H.
bonariensis to translocate nutrients and water, evaluating possible ecological and
evolutionary consequences of these abilities. He discovered that H. bonariensis can translocate nitrogen acquired by ramets growing in areas of high concentration to ramets growing in areas of low concentration, thus allowing expansion into environments where resources are patchy or nonexistent (Evans 1988). In another study, Evans (1991) was
31 able to quantitatively access the fitness related benefits of nutrient and water translocation by measuring increases in total biomass, ramet proliferation and seed production. Evans
(1992b) also documented that H. bonariensis clones exhibit an integrated morphological response to a resource environment (the dune) which is variable in space and time.
Hydrocotyle bonariensis has been observed to expand into salt marsh communities from surrounding dune systems with no apparent ill effects due to contact with saline water (Evans and Whitney 1992). In an attempt to explain this observation, the authors conducted a field experiment in which they severed some rhizomes of H. bonariensis and did not sever others. They found that ramets attached to severed rhizomes exhibited high mortality while ramets attached to non-severed rhizomes were not affected by saline conditions. The authors concluded that translocation of water from ramets growing in dune systems allowed ramets of H. bonariensis to grow into the salt marsh. Finally, Evans and Cain (1995) demonstrated that H. bonariensis can respond to the environment by altering branching patterns, internodal distance and direction of rhizome growth; essentially the plant can “forage” for resources.
In other studies, Overdieck and Strain (1981) discovered that H. bonariensis growing at three distinct sites on Shackleford Banks, North Carolina were essentially ecotypes adapted to their local environment. Longstreth et al. (1981) found that leaves of
H. bonariensis grown under high irradiances were smaller, thicker, reached maximum size more quickly and had higher photosynthetic rates than did leaves grown under low irradiances. Haddad and Mazzafera (1999) conducted an investigation in which they grew cuttings of H. bonariensis in different concentrations of sodium chloride. They observed that regardless of the concentration, all sodium chloride solutions induced a
32 decrease in fresh and dry weights and chlorophyll content of leaves. Finally, Knight and
Miller (2004) used reciprocal transplants to address the existence and possible causes of local adaptation in H. bonariensis plants growing on Saint George Island, Florida. They reported evidence for local adaptation and concluded that this adaptation was related to interactions with other dune plants.
Iva imbricata
Iva imbricata is a woody C3 shrub with succulent leaves found along the coasts of
southern Virginia to the Florida Keys, Gulf Coast of the United States and on beaches of
Caribbean islands (Jackson 1960). The plant can grow to heights of 1 m and widths of
3 m (Radford et al. 1968). As a seedling, I. imbricata coinhabits the driftline with A. pumilus and C. edentula. Winter storms usually remove all vegetation from this habitat including I. imbricata seedlings. Seedlings that are landward (higher elevation) of winter
storm overwash can survive into multiple growing seasons trapping sand and acting as
dune builders (Rogers and Nash 2003). Thus on Topsail Island, I. imbricata essentially
defines the beginning of permanent vegetation known as the foredune and/or primary
dune (Frankenberg 1997).
There are only four studies that have been conducted with I. imbricata. Colosi
and McCormick (1978) extensively documented the population structure of I. imbricata
in five different habitats on Smith Island, North Carolina. They found that seed
production and seedling emergence were greatest in the foredune habitat, but that harsh
physical factors resulted in a high mortality rate so much so that populations were
maintained via asexual reproduction. In habitats where environmental conditions were
33 more ameliorated, seedling survival was much higher. Seed source then became the
limiting factor for population numbers.
In a series of studies, Franks investigated inter and intraspecific facultative interactions of I. imbricata on the sand dunes of Georgia and Florida. In one study, he
found that interactions were facultative for survival but competitive for biomass
production and that the presence or absence of neighbors was more important than
whether the neighbors were conspecifics or not (Franks 2003a). In a second study,
Franks and Peterson (2003) determined that facilitation increased with increasing
disturbance severity but that species richness had little effect. In a third study, Franks
(2003b) found support for the nucleation hypothesis in that nurse plants provided microsites for the accumulation and germination of seeds and subsequent seedling growth of I. imbricata.
Literature Cited
Adair, J.A., T.R. Higgins and D.L. Brandon. 1990. Effects of fruit burial depth and wrack on the germination and emergence of the strandline species Cakile edentula (Brassicaceae). Bulletin of the Torrey Botanical Club. 117:138-142.
Adger, W.N., T.P. Hughes, C. Folke, S.P. Carpenter and J. Rockstrom. 2005. Social- ecological resilience to coastal disasters. Science. 309:1036-1039.
Alexander, J. and J. Lazell. 2000. Ribbon of sand. The University of North Carolina Press, Chapel Hill, NC (USA).
Alpha, C.G., D.R. Drake and G. Goldstein. 1996. Morphological and physiological responses of Scaevola sericea (Goodeniaceae) seedlings to salt spray and substrate salinity. American Journal of Botany. 83:86-92.
Au, S.F. 1974. Vegetation and ecological processes on Shackelford Banks, North Carolina. National Park Service Scientific Monograph Series. Number 6.
Art, H.W., R.H. Bormann, G.K. Boigt and G.M. Woodwell. 1974. Barrier island forest ecosystem: role of meteorological nutrient inputs. Science. 184:60-62.
34 Barbour, M.G. 1970. Germination and early growth of the strand plant Cakile maritma. Bulletin of the Torrey Botanical Club. 97:13-22.
Barbour, M.G. 1978. Salt spray as a microenvironmental factor in the distribution of beach plants at Point Reyes, California. Oecologia. 32:213-224.
Barbour, M.G. and T.M. DeJong. 1977. Response of West Coast beach taxa to salt spray, seawater inundation, and soil salinity. Bulletin of the Torrey Botanical Club. 104:29-34.
Barbour, M.G., T.M. DeJong and B.M. Pavlik. 1985. Marine beach and dune plant communities in B.F. Chabot and H.A. Mooney [editors], Physiological Ecology of North American Plant Communities. Pages 296-322. Chapman and Hall, New York, New York (USA).
Barbour, M.G. and J.E. Rodman. 1970. Saga of the West Coast sea-rockets: Cakile edentula ssp. californica and C. maritima. Rhodora. 72:370-386.
Barnes, J. 2001. North Carolina’s hurricane history (3rd edition). The University of North Carolina Press, Chapel Hill, NC (USA).
Baskin, J.M. and C.C. Baskin. 1998. Scientific note: seed dormancy and germination in the rare plant species Amaranthus pumilus. Castanea. 63:493-494.
Billings, W.D. 1985. The historical development of physiological plant ecology in B.F. Chabot and H.A. Mooney [editors], Physiological Ecology of North American Plant Communities. Pages 1-15. Chapman and Hall, New York, New York (USA).
Boyce, S.G. 1954. The salt spray community. Ecological Monographs. 24:29-67.
Boyd, R.S. 1988. Herbivory and species replacement in the West Coast searockets (Cakile, Brassicaceae). The American Midland Naturalist. 119: 304-317.
Boyd, R.S. 1991. Population biology of West Coast Cakile maritima: effects of habitat and predation by Peromyscus maniculatus. Canadian Journal of Botany. 69:2620-2630.
Boyd, R.S. and M.G. Barbour. 1986. Relative salt tolerance of Cakile edentula (Brassicaceae) from lacustrine and marine beaches. American Journal of Botany. 73:236-241.
Boyd, R.S. and M.G. Barbour. 1993. Replacement of Cakile edentula by C. maritima in the strand habitat of California. The American Midland Naturalist. 130:209-228.
CBIN (Coastal Barrier Island Network). http://www.coastalbarrierisland.org/
35
Chrylser, M. 1904. Anatomical notes on certain strand plants. Botanical Gazette. June:461-464.
Cleary, W.J. and P.E. Hosier. 1979. Geomorphology, washover history and inlet zonation: Cape Lookout, NC to Bird Island, NC in S. Leatherman, [editor], Barrier Islands. Pages 237-271. Academic Press, New York, New York (USA).
Cleland, E.E., I. Chuine, A. Menzel, H.A. Mooney and M.D. Schwartz. 2007. Shifting plant phenology in response to global change. Trends in Ecology and Evolution. 22:357-365.
Clements, S. and C. Mangels. 1990. Report on Amaranthus pumilus surveys in New York State 1990. New York Natural Heritage Program. New York State Department of Environmental Conservation, New York (USA).
Cody, M.L. and T.W.D. Cody. 2004. Morphology and spatial distribution of alien sea- rockets (Cakile ssp.) on South Australian and Western Canadian beaches. Australian Journal of Botany. 52:175-183
Colosi, J.C. and J.F. McCormick. 1978. Population structure of Iva imbricata in five coastal dune habitats. Bulletin of the Torrey Botanical Club. 105:175-186.
Cowles, H.C. 1899. The ecological relations of the vegetation on sand dunes of Lake Michigan. The Botanical Gazette. 27:95-117, 167-202, 281-308, 361-391.
Crawford, R.M.M. 2008. Plants at the margin. Cambridge University Press, Cambridge (GBR).
DeBeaumont, E. 1845. Lecons de geologie pratique. Paris (FRA).
DeJong, T.M. 1978a. Comparative gas exchange of four California beach taxa. Oecologia. 34:343-351.
DeJong, T.M. 1978b. Comparative gas exchange and growth responses of C3 and C4 beach species grown at different salinities. Oecologia. 36:59-68.
DeJong, T.M. 1979. Water and salinity relations of California beach species. Journal of Ecology. 67:647-663.
Dolan, R., B. Hayden and H. Lins. 1980. Barrier islands. American Scientist. 68:16-25.
Donohue, K. 1997. Seed dispersal in Cakile edentula var. lacustris: decoupling the fitness effects of density and distance from the home site. Oecologia. 110:520- 527.
36 Donohue, K. 1998. Maternal determinants of seed dispersal in Cakile edentula: fruit, plant and site traits. Ecology. 79:2771-2788.
Donohue, K. 2003. The influence of neighbor relatedness on multilevel selection in the Great Lakes sea rocket. American Naturalist. 162:77-92
Donohue, K. 2004. Density-dependent multilevel selection in the Great Lakes sea rocket. Ecology. 85:180-191.
Dubois, S.J. 1977. Comparative ecophysiology of C3 and C4 sand dune plant species of the Georgia coast. Master’s Thesis. University of Georgia, Athens, Georgia (USA).
Dudley, S.A. 1996a. Differing selection on plant physiological traits in response to environmental water availability: a test of adaptive hypotheses. Evolution. 50:92-102.
Dudley, S.A. 1996b. The response to differing selection on plant physiological traits: evidence for local adaptation. Evolution. 50:103-110.
Dudley, S.A. and A.L. File. 2007. Kin recognition in an annual plant. Biology Letters. 3:435-438.
Ehrenfeld, J.G. 1990. Dynamics and processes of barrier island vegetation. Aquatic Sciences. 2:437-480.
Elsner, J.B., J.P. Kossin and T.H. Jagger. 2008. The increasing intensity of the strongest tropical cyclones. Nature. 455:92-95.
Evans, J.P. 1988. Nitrogen translocation in a clonal dune perennial, Hydrocotyle bonariensis. Oecologia. 77:64-68.
Evans, J.P. 1991. The effect of resource integration on fitness related traits in a clonal dune perennial, Hydrocotyle bonariensis. Oecologia. 86:268-275.
Evans, J.P. 1992a. Seedling establishment and genet recruitment in a population of a clonal dune perennial. Barrier Island Ecology of the Mid-Atlantic Coast: a Symposium. Technical Report NPS/SERCAHA/NRTR-93/04.
Evans, J.P. 1992b. The effect of local resource availability and clonal integration on ramet functional morphology in Hydrocotyle bonariensis. Oecologia. 89:265- 276.
Evans, J.P. and M.L. Cain. 1995. A spatially explicit test of foraging behavior in a clonal plant. Ecology. 76:1147-1155.
37 Evans, J.P. and S. Whitney. 1992. Clonal integration across a salt gradient by a nonhalophyte, Hydrocotyle bonariensis (Apiaceae). American Journal of Botany. 79:1344-1347.
Feagin, R.A., W.K. Smith, N.P. Psuty, D.R. Young, J.C. Gibeaut, M.L. Martinez, K.F. Nordstrom, N.L. Jackson, G.A. Carter, J.N. Gemma, R.E. Koske, D.H. Thomas, J.C. Whitehead and K.L. Lucas. 2009. Barrier islands: coupling anthropogenic stability with ecological sustainability. Journal of Coastal Research (in press).
Fisher, J.J. 1968. Barrier island formation: discussion. Geological Society of America Bulletin. 79:1421-1426.
Franks, S.J. 2003a. Competitive and facultative interactions within and between two species of coastal dune perennials. Canadian Journal of Botany. 81:330-337.
Franks, S.J. 2003b. Facilitation in multiple life-history stages: evidence for nucleated succession in coastal dunes. Plant Ecology. 168:1-11.
Franks, S.J. and C.J. Peterson. 2003. Burial disturbance leads to facilitation among coastal dune plants. Plant Ecology. 168:13-21.
Frankenberg, D. 1995. The Nature of the Outer Banks. The University of North Carolina Press, Chapel Hill, NC (USA).
Frankenberg, D. 1997. The Nature of North Carolina’s Southern Coast. The University of North Carolina Press, Chapel Hill, NC (USA).
Gedge, K.E. and M.A. Maun. 1992. Effects of simulated herbivory on growth and reproduction of two beach annuals, Cakile edetula and Corispermum hyssopifolium. Canadian Journal of Botany. 70:2467-2475.
Gilbert, G.K. 1885. The topographic features of southeastern Queensland. Australian Geographer. 9:207-217.
Glaeser, J.D. 1978. Global distribution of barrier islands in terms of tectonic setting. Journal of Geology. 86:283-297.
Godfrey, P.J. 1976. Barrier islands of the East Coast. Oceanus. 19:27-40.
Goldenberg, S.B., C.W. Landsea, A.M. Mestas-Nunez and W.M. Gray. 2001. The recent increase in Atlantic hurricane activity: causes and implications. Science. 293:474-479.
Greaver, T.L. and L.L da S. Sternberg. 2006. Linking marine resources to ecotonal shifts of water uptake by terrestrial dune vegetation. Ecology. 87:2389-2396.
38 Gutshick, V.P. and H. BassiriRad. 2003. Extreme events as shaping physiology, ecology and evolution of plants: toward a unified definition and evaluation of their consequences. New Phytologist. 160:21-42.
Guy, R.D., P.G. Warne and D.M. Reid. 1989. Carbon isotope ratios of C3 halophytes in P.W. Rundel, J.R. Ehleringer and K.A. Nagy [editors.], Stable isotopes in ecological research. Pages 55-75. Springer-Verlag, New York, NY (USA).
Haddad, C.R.B. and P. Mazzafera. 1999. Sodium chloride-induced leaf senescence in Hydrocotyle bonariensis Lam. and Foeniculum vulgare L. Brazilian Archives of Biology and Technology. 42:161-168.
Hamilton, R.D. 2000. Techniques for the propagation of Amranthus pumilus. Annual Report of the Waddell Mariculture Center, Bluffton, South Carolina (USA).
Hancock, T.E. and P.E. Hosier. 2003. Ecology of the threatened species Amaranthus pumilus Rafinesque. Castanea. 68:236-244.
Hayden, B.P., R.D. Dueser, J.T. Callahan and H.H. Shugart. 1991. Long-term research at the Virigina Coastal Reserve. Bioscience. 41:310-318.
Hayden, B.P. and N.R. Hayden. 2003. Decadal and century-long storminess changes at long-term ecological research sites in D. Greenland, D.G. Goodin and R.C. Smith [editors], Climate variability and ecosystem climate variability and response at long-term ecological research sites. Pages 262-285. Oxford University Press, New York, NY (USA).
Holgate, S.J. and P.L. Woodworth. 2004. Evidence for enhanced sea level rise during the 1990’s. Geophysical Research Letters. 31:L07305.
Hosier, P.E. and W.J. Cleary. 1977. Cyclic geomorphic patterns on an overwash dominated barrier island in Southeastern North Carolina. Environmental Geology 2:23-31.
Hoyt, J.H. 1967. Barrier island formation. Geological Society of America Bulletin. 78:1125-1136.
Hoyt, J.H. and J.R. Hails. 1967. Deposition and modification of Pleistocene shoreline sediments in coastal Georgia. Science. 155:1541-1543.
Ignaciuk, R. and J.A. Lee. 1980. The germination of four annual strand-line species. New Phytologist. 84:581-591.
Intergovernmental Panel on Climate Change (IPCC). 2007. Climate Change 2007: Synthesis Report.
39 Ishikawa, S., T. Oikawa and S. Furukawa. 1990. Photosynthetic characteristics and water use efficiency of three coastal dune plants. Ecological Research. 5:377- 391.
Ishikawa, S., T. Oikawa and S. Furukawa. 1991. Responses of photosynthesis, leaf conductance and growth to different salinities in three coastal dune plants. Ecological Research. 6:217-226.
Ishikawa, S., S. Furukawa and T. Oikawa. 1995. Zonal plant distribution and edaphic and micrometeorlogical conditions on a coastal sand dune. Ecological Research. 10:259-266.
Ishikawa, S., S. Furukawa and T. Oikawa. 1996. Photosynthetic responses to drought conditions in three coastal dune plants in relation to their zonal distribution. Australian Journal of Botany. 44:381-391.
Jackson, R.C. 1960. A revision of the genus Iva L. University of Kansas Science Bulletin. 41:793-896.
Jentsch, A., J. Kreyling and C. Beierkuhnlein. 2007. A new generation of climate- change experiments: events not trends. Frontiers in Ecology and the Environment. 7:365-374.
Johnson, D.W. 1919. Shore processes and shoreline development. John Wiley and Sons, New York, New York (USA).
Kearney, T.H. 1900. The plant covering of Ocracoke Island: a study in the ecology of the North Carolina strand vegetation. United States National Herbarium, Contributions. 5:321-585.
Kearney, T.H. 1904. Are plants of sea beaches and dunes true halophytes? Botanical Gazette. 37:424-436.
Keddy, P.A. 1981. Experimental demography of the sand dune annual, Cakile edentula, growing along an environmental gradient in Nova Scotia. Journal of Ecology. 69:615-630.
Keddy, P.A. 1982. Population ecology on an environmental gradient: Cakile edentula on a sand dune. Oecologia. 52:348-355.
Keinath, A.P., A.E. Strand, R.D. Hamilton. 2003. First report of white rust caused by Albugo bliti on seabeach amaranth in the United States. Plant Diseases. 87:602.
Knight, T.M. and T.E. Miller. 2004. Local adaptation within a population of Hydrocotyle bonariensis. Evolutionary Ecology Research. 6:103-114.
40 Lambers, H., F.S. Chapin III and T.L. Pons. 1998. Plant Physiological Ecology. Springer, New York, New York (USA).
Longstreth, D.J., T.L. Hartsock and P.S. Nobel. 1981. Light effects on leaf development and photosynthetic capacity of Hydrocotyle bonariensis Lam. Photosynthesis Research. 2:95-104.
Mann, M.E., J.D. Woodruff, J.P. Donnelly and Z. Zhang. 2009. Atlantic hurricanes and climate over the past 1,500 years. Nature. 460:880-883.
Marcone, M.F. 2000. First report of the characterization of the threatened plant species Amaranthus pumilus (seabeach amaranth). Journal of Agricultural Food Chemistry. 48:378-382.
Martinez, M.L. and P. Moreno-Casasola. 1993. Survival of seedling cohorts of a tropical legume on a sand dune system along the Gulf of Mexico: influence of germination date. Canadian Journal of Botany. 71:1427-1433.
Martinez, M.L., G. Vazquez, D.A. White, G. Thivet and M. Brengues. 2002. Effect of burial by sand and inundation by fresh and seawater on seed germination of five tropical beach species. Canadian Journal of Botany. 80:416-424.
Maun, M.A., R.S. Boyd and L. Olson. 1990. The biological flora of coastal dunes and wetlands. 1. Cakile edentula (Bigelow) Hooker. Journal of Coastal Research. 6:137-156.
Maun, M.A. and J. Lapierre. 1986. Effects of burial by sand on seed germination and seedling emergence of four dune species. American Journal of Botany. 73:450- 455.
Miyanishi, K. and E.A. Johnson. 2007. Coastal dune succession and the reality of dune processes in E.A. Johnson and K. Miyanishi [editors], Plant Disturbance Ecology. Pages 249-282. Academic Press, Burlington, MA (USA).
Mooney, H.A. 1980. Photosynthetic plasticity of populations of Heliotropium curassavicum L. originating from different thermal regimes. Oecologia. 45:372- 376.
Mooney, H.A., C. Field, W.E. Williams, J.A. Berry and O. Bjorkman. 1983. Photosynthetic characteristics of plants of a California cool coastal environment. Oecologia. 57:38-42.
Nash, S. 2008. Wetlands, icecaps, unease: sea-level rise and Mid-Atlantic shorelines. BiosScience 58:919-923.
NOAA Coastal Services Center.
41 http://www.csc.noaa.gov/beachnourishment/html/geo/barrier.htm
Norden, D.S., F.A. Blazich, S.L. Warren and D.L. Nash. 2007. Seed germination of seabeach amaranth (Amaranthus pumilus) in response to temperature, light and gibberellin A3 treatments. Journal of Environmental Horticulture. 25:105-108.
Oosting, H.J. 1945. Tolerance to salt spray of plants of coastal dunes. Ecology. 26:85- 89.
Oosting, H.J. 1954. Ecological processes and vegetation of the maritime strand in the southeastern United States. Botanical Review. 20:226-262
Oosting, H.J. and W.D. Billings. 1942. Factors affecting vegetational zonation on coastal dunes. Ecology. 23:131-142.
Otvos, E.G. 1970. Development and migration of barrier islands, northern Gulf of Mexico. Geological Society of America Bulletin. 81:241-246.
Overdieck, D. and B.R. Strain. 1981. Effects of atmospheric humidity on net photosynthesis, transpiration and stomatal resistance of Hydrocotyle umbellata L. and Hydrocotyle bonariensis Lam. International Journal of Biometeorology. 25:29-38.
Pavlik, B.M. 1983. Nutrient and productivity relations of the dune grasses Ammophila arenaria and Elymus mollis. Oecologia. 57:227-232.
Payne, A.M. and M.A. Maun. 1984. Reproduction and survivorship of Cakile edentula var. lacustris along the Lake Huron shoreline. The American Midland Naturalist. 111:86-95.
Pearcy, R.W. 1976. Temperature responses of growth and photosynthesic CO2 exchange rates in coastal and desert races of Atriplez lentiformis. Oecologia. 26:245-255.
Pemadasa, M.A., P. Greig-Smith and P.H. Lovell. 1974. A quantitative description of the distribution of annuals in the dune system at Aberffraw, Anglesey. Journal of Ecology. 62:379-402.
Pemadasa, M.A. and P.H. Lovell. 1974. The mineral nutrition of some dune annuals. Journal of Ecology. 62:647-657.
Pemadasa, M.A. and P.H. Lovell. 1975. Factors controlling germination of some dune annuals. Journal of Ecology. 63:41-59.
Perumal, V.J. and M.A. Maun. 2006. Ecophysiological response of dune species to
42 experimental burial under field and controlled conditions. Plant Ecology. 184:89-104.
Parmesan, C. 2006. Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution and Systematics. 37:637-669.
Pike, D.A. and J.C. Stiner. 2007. Sea turtle species vary in their susceptibility to tropical cyclones. Oecologia. 153:471-478.
Pilkey, O.H. and J.A.G. Cooper. 2004. Society and sea level rise. Science. 303:1781- 1782.
Pilkey, O.H., W.J. Neal, S.R. Riggs, C.A. Welsh, D.M. Bush, D.F. Pilkey, J. Bullock and B.A. Cowan. 1998. The North Carolina shore and its barrier islands: restless ribbons of sand. Duke University Press, Durham, NC (USA).
Pilkey, O.H. and L. Pilkey-Jarvis. 2007. Useless arithmetic: why environmental scientists can’t predict the future. Columbia University Press, New York, NY (USA).
Radford, A.E., H.E. Ahles and C.R. Bell. 1968. Manual of the Vascular Flora of the Carolinas. The University of North Carolina Press. Chapel Hill, North Carolina (USA).
Ramsey, S., W. Tyndall and C. Lea. 2000. Scientific note: the federally threatened Amranthus pumilus Rafinesque (seabeach amaranth) rediscovered on Assateague Island after 31 years. Castanea. 65:165-167.
Ranwell, D.S. 1972. Ecology of Salt Marshes and Sand Dunes. Chapman and Hall, London (GBR).
Riggs, S.R. and D.V. Ames. 2006. Effect of storms on barrier island dynamics, Core Banks, Cape Lookout National Seashore, North Carolina, 1960-2001. United States Geological Survey Scientific Investigation Report 2006-5309.
Rogers, S. and D. Nash. 2003. The Dune Book. North Carolina Sea Grant, Raleigh, NC (USA).
Rosenfeld, K.M. 2004. Ecology of Bird Island North Carolina, an uninhabited, undeveloped barrier island. Master’s Thesis. North Carolina State University, Raleigh, North Carolina (USA).
Salisbury, E. 1952. Downs and Dunes. Their plant life and its environment. Bell, London (GBR).
Schat, H. and M. Scholten. 1986. Effects of salinity on growth, survival and life history
43 of four short-lived pioneers from brackish dune slacks. Acta Ecologica. 7:221- 231.
Schlacher, T.A., D.S. Schoeman, J. Dugan, M. Lastra, A. Jones, F. Scapini and A. McLachlan. 2008. Sandy beach ecosystems: key features, sampling issues, management challenges and climate change impacts. Marine Ecology. 29:70-90.
Schwartz, M.L. 1971. The multiple causality of barrier islands. Journal of Geology. 79:91-94.
Sellers, J.D. and C.L. Jolls. 2007. Habitat modeling for Amaranthus pumilus: an application of Light Detection and Randing (LIDAR) data. Journal of Coastal Research. 23:1193-1202.
Silander, J.A. and J. Antonovics. 1982. Analysis of interspecific interactions in a coastal plant community – a perturbation approach. Nature. 298:557:560.
Snyder, R.A. and C.L. Boss. 2002. Recovery and stability in barrier island plant communities. Journal of Coastal Research. 18:530-536.
Stallings, J.A. and A.J. Parker. 2003. The influence of complex systems interactions on barrier island dune vegetation pattern and process. Annals of the Association of American Geographers. 93: 13-29.
Stallman, D.A. 2004. Echoes of Topsail. Carlisle Printing, Sugarcreek, OH (USA).
Starr, A. 1912. Comparative anatomy of dune plants. Botanical Gazette. October:264- 305.
Stick, D. 1952. Graveyard of the Atlantic. Chapel Hill Press, Chapel Hill, NC (USA).
Stick, D. 1958. The Outer Banks of North Carolina. Chapel Hill Press, Chapel Hill, NC (USA).
Stive, M.J. and E.S. Hammer-Klose. 2004. How important is global warming for coastal erosion? Climatic Change. 64:27-39.
Strand, A.E. 2002. Characterization of the genetic structure in Amaranthus pumilus. Annual Report of the Department of Biology, College of Charleston, South Carolina (USA).
Thompson, D.M., G.P. Shaffer and J.A. McCorquodale. 2001. A potential interaction between sea-level rise and global warming: implications for coastal stability on the Mississippi River Deltaic Plain. Coastal Management. 32:49-59.
Turner, M.G., V.H. Dale and E.H. Everham III. 1997. Fire, hurricanes and volcanoes:
44 comparing large disturbances. Bioscience. 47:758-768.
Tyndall, R.W., A.H. Teramura, C.L. Mulchi and L.W. Douglas. 1986a. Seed burial effect on species presence along a mid-Atlantic beach. Canadian Journal of Botany. 64:2168-2170.
Tyndall, R.W., A.H. Teramura and L.W. Douglas. 1986b. Potential role of soil moisture deficit in the distribution of Cakile edentula. Canadian Journal of Botany. 64:2789-2791.
Ungar, I.A. 1991. Germination ecology of halophytes in D.N. Sena and K. Rajpurohit [editors], Contributions to the ecology of halophytes. Junk, The Hague (DEU).
United States Army Corps of Engineers, Wilmington District Amaranthus pumilus surveys. 1992-1995.
United States Fish and Wildlife Service. 1993. Endangered and threatened wildlife and plants; Amaranthus pumilus (seabeach amaranth) determined to be threatened. Federal Register 58(65):18035-18041.
van der Valk, A.G. 1974a. Environmental factors controlling the distribution of forbs on foredunes in Cape Hatteras National Seashore. Canadian Journal of Botany. 52:1057-1073.
van der Valk, A.G. 1974b. Mineral cycling in coastal foredune plant communities in Cape Hatteras National Seashore. Ecology. 55:1349-1358. van der Valk, A.G. 1975. The floristic composition and structure of foredune plant communities of Cape Hatteras National Seashore. Chesapeake Science. 16:115- 126.
van der Valk, A.G. 1977. The macroclimate and microclimate of coastal foredune grasslands in Cape Hatteras National Seashore. International Journal of Biometeorology. 21:227-237.
van Schoik, D.R. and S. Antenen. 1993. Final Report, 1993, Amaranthus pumilus, Long Island, New York. Long Island Chapter of The Nature Conservancy, New York (USA).
Watkinson, A.R. 1978. The demography of a sand dune annual: Vulpia fascuculata. II. The dynamics of seed populations. Journal of Ecology. 66:35-44.
Watkinson, A.R. and J.L. Harper. 1978. The demography of a sand dune annual: Vulpia fascuculata. I. The natural regulation of populations. Journal of Ecology. 66:15- 33.
45 Weakley, A.S. and M.A. Bucher. 1992. Status survey of seabeach amaranth (Amaranthus pumilus Rafinesque) in North and South Carolina. Report to the North Carolina Plant Conservation Program and Endangered Species Field Office, North Carolina (USA).
Wells, B.W. 1939. A new forest climax: the salt spray climax of Smith Island, N.C. Bulletin of the Torrey Botanical Club. 66: 631-634.
Woodhouse, Jr. W.W. 1978. Dune building and stabilization with vegetation. Special Report Number 3. United States Army Corps of Engineering Coastal Research Center. Fort Belvoir, Virginia.
Woodhouse, Jr. W.W and R.E. Hanes. 1966. Dune stabilization with vegetation on the Outer Banks of North Carolina. Soils Information Series 8. Department of Soil Science, North Carolina State University, Raleigh, North Carolina (USA).
Woodhouse, Jr., W.W., E.D. Seneca and S. Broome. 1976. Ten years of development of man-initiated coastal barrier dunes in North Carolina. North Carolina Agricultural Experimental Station Bulletin. 453:1-53.
Woodhouse, Jr., W.W., E.D. Seneca and A.W. Cooper. 1968. Use of sea oats for dune stabilization in the southeast. Shore and Beach. 36:15-21.
Zhang, J. 1993. Seed dimorphism in relation to germination and growth of Cakile edentula. Canadian Journal of Botany. 71:1231-1235
Zhang, J. 1994. Early seedling development in relation to seed mass and morph in Cakile edentula. Canadian Journal of Botany. 72:402-406.
Zhang, J. 1996. Interactive effects of soil nutrients, moisture and sand burial on the development, physiology, biomass and fitness of Cakile edentula. Annals of Botany. 78:591-598.
Zhang, J. and M.A. Maun. 1992. Effects of burial in sand on the growth and reproduction of Cakile edentula. Ecography. 15:296-302.
Zhang, J. and M.A. Maun. 1994. Potential for seed bank formation in seven Great Lakes sand dune species. American Journal of Botany. 81:387-394.
Zhang, K., B.C. Douglas and S.P. Leatherman. 2004. Global warming and coastal erosion. Climatic Change. 64:41-58.
46 CHAPTER III
LEAF FORM AND FUNCTION: TESTING A MODEL
Introduction
The question of how leaf form (internal anatomy, external morphology and leaf
orientation) affects leaf function has intrigued plant biologists since the early part of the
20th century (Salisbury and Ross 1992, Barbour et. al 1999). In particular, researchers
have been keenly interested in better understanding how plants can maximize
photosynthesis while minimizing structural costs in a variety of habitats across a gradient
of stresses (Lambers et al. 1998, Nobel 1999). Past studies have focused on documenting
photosynthetic response of leaves illuminated on the adaxial (upper surface) versus
abaxial (lower surface) leaf surface (Moss 1964, Oya and Laisk 1975, Terashima 1986,
Day et al. 1990, Proietti and Palliotti 1997) gross internal anatomy and chemistry of the
leaf (Esau 1972, Nobel et al. 1975, Mooney and Gulmon 1979, Levitt 1980, Longstreth
1981. Evans 1995, Evans 1999, Sun and Nishio 2001 – and references therein), and stomatal frequency in relation to leaf anatomy (Parkhurst 1978, Mott et al. 1982, Smith et al. 1998, Woodward et al. 2002).
More recently, questions concerning leaf orientation impacts on anatomy,
physiology and resultant photosynthetic rates have been posed (DeLucia et al. 1991,
Poulson and DeLucia 1993, Smith el al. 1998, Evans and Vogelmann 2006, Soares et al.
2007). The importance of direct versus diffuse light has also begun to be addressed
(Johnson and Smith 2006, Brodersen and Vogelmann 2007, Brodersen et al. 2008). New
47 techniques employing fibre optic, chlorophyll fluorescence, and photo-acoustic
technologies have given researchers the ability to observe leaf anatomy at the cell and
chloroplast level providing the opportunity for detailed experiments addressing the
relationship of leaf form to function (Evans 1999, Han et al. 1999, Yano and Terashima
2001, Yano and Terashima 2004, Evans and Vogelmann 2003, Evans and Vogelmann
2006, Wang et al. 2008 – and references therein).
Regardless of the approach employed or technologies utilized, the goal of leaf
form and function research is to understand how plants maximize photosynthesis given
developmental, structural and energy constraints. To this end, Smith et al. (1997)
proposed a model that describes how plants maximize photosynthesis per unit leaf
biomass by regulating light and CO2 gradients inside the leaf. The model predicts leaf form and orientation in relation to a gradient of environmental stresses. According to the model, as environmental stresses increase (including sunlight), leaf anatomy changes from monotypic layers consisting of spongy mesophyll (i.e. a unifacial leaf) to differentiated layers with development of adaxial palisade mesophyll and abaxial spongy mesophyll (i.e. a bifacial leaf). As stresses continue to increase, an abaxial palisade layer begins to develop making the leaf more symmetrical. At the highest levels of stress, leaves become cylindrical with the internal anatomy reverting back to a monotypic layer of spongy mesophyll cells. The cylindrical shape of the leaf provides for a large overlap between the internal light and CO2 diffusion gradients resulting in increased
photosynthesis per unit leaf biomass. The cylindrical leaf shape (versus a planar leaf)
reduces the stressful effects of sunlight due to the cosine effect (Nobel 1999). The model also predicts that leaf form will proceed from a horizontal to a vertical orientation as
48 environmental stresses increase. In lower stress environments, leaves are predicted to be
hypostomatous (i.e. stomata only present on the abaxial surface) becoming
amphistomatous (i.e. stomata present on both abaxial and adaxial surfaces) as
environmental stresses increase. Importantly, this conceptual model of leaf form includes
the idea that leaf morphology and anatomy is dictated by leaf orientation and the resulting
sunlight exposure on both leaf sides, including the total amounts on each side, as well as
the ratio of adaxial/abaxial incidence (Smith et al. 1997, 1998).
A number of studies provide support for the model’s predictions in relation to leaf
anatomy (Nobel et al. 1975, Day et al. 1990, Evans 1995, Rocas and Scarano 2001,
Oguchi et al. 2003), leaf orientation (DeLucia et al. 1991, Poulson and DeLucia 1993,
Evans and Vogelmann 2003, Greaver and Herbert 2004), and stomatal frequency and
position (Mott et al. 1982, Boardman et al. 1991, Woodward et al. 2002, Wang et al.
2008). However, the majority of these studies were conducted on agricultural species or
on natural species grown in the greenhouse and artificially manipulated (with two notable
exceptions – Nobel et al. 1975, Greaver and Herbert 2004). Smith et al. (1998) is the
only study that has directly tested the model’s prediction and these tests were limited to
species living in two stressful habitats (the United States Rocky Mountain subalpine and
five Australian communities).
The leaf form versus environmental stress model awaits further validation with
species from a variety of habitats with different stress levels according to quality and
quantity. An excellent test of the model can be made with barrier island (BI) beach species of the east coast of the United States. Plants growing on BI beaches face numerous abiotic stresses that limit growth. Stresses such as high solar radiation, salt
49 spray, sand abrasion, low nutrient substrates, and salt water overwash have been documented to affect leaf form (see Erhenfeld 1990 for a review) and assumedly leaf function. Due to the characteristics of this harsh and highly transient environment, BI beach species should provide a robust test of the model’s breadth and applicability.
In the present study, four species representing distinct functional plant groups (as
defined by Shao et al. 1996, Crawford 2008) were chosen to test the predictions of the
leaf form/function model proposed by Smith et al. (1997).
Materials and Methods
Study Site
Topsail Island is a low topographic relief, 42 km long BI that varies in width from
150 to 500 m located approximately 40 km northeast of Wilmington, North Carolina
(Stallman 2004). The island is extensively developed with single family homes along
almost its entire length (Frankenburg 1997). The study site was located on the
southwestern end of the island (34o 20’ 50” N, 77o 39’ 5” W) adjacent to New Topsail
Inlet. Due to migration of the inlet to the southwest at an average rate of 35 m per year,
an extensive beach and dune environment extends approximately 1-2 km from the inlet to
the first beach home.
Species
Amaranthus pumilus (Rafinesque) is a pioneering C4 annual species that inhabits
the driftline and foredune area of the BI beach (Weakley and Bucher 1992). The plant
has a prostrate growth form, succulent leaves and pink to reddish stems. As a result of
population decline due to habitat loss, A. pumilus was listed as federally threatened in
1993 (Weakley and Bucher 1992, United States Fish and Wildlife Service 1993). Cakile
50 edentula (Bigelow) Hooker is a pioneering C3 annual species that has an upright growth
form and succulent leaves (Radford et al. 1968). The plant is common within its range
(Barbour and Rodman 1970) and unlike A. pumilus, C. edentula can persist into a second
growing season in moderate climates (Barbour and Rodman 1970, Boyd and Barbour
1993, Cody and Cody 2004). Hydrocotyle bonariensis is a C3 perennial species whose
seeds germinate in swales located landward of the primary dune on BI beaches (Evans
1992). The plants can grow seaward into the foredune via rhizomes (Evans 1992).
Leaves are peltate, vary in width from 4 to 12 cm and senesce in winter with the rhizomes
persisting underground until the next growing season (Radford et al. 1968). Iva
imbricata is a succulent leaved, woody C3 shrub that can grow to heights of 1 m and
widths of 3 m (Radford et al. 1968). As a seedling, I. imbricata coinhabits the driftline with A. pumilus and C. edentula.
The Sunlight Environment
Continuous measurements of Photosynthetically Active Radiation (PAR) were
taken from June 2002 until June 2004 using a LI-190 Quantum Sensor (Li-Cor, Lincoln
Nebraska) mounted on a 1.5 m wooden pole (10 cm X 10 cm) interfaced with a HOBO data logger via a Universal Transconductance Amplifier (EME Systems, Berkley CA).
Individual measurements of PAR where taken every 2-3 hours from dawn until dusk approximately one day per month from June 2002 until June 2004. For individual PPF measurements, a LI-190 Quantum Sensor (Li-Cor, Lincoln, Nebraska) interfaced with a
Li-250A hand-held light meter (Li-Cor, Lincoln, Nebraska) was used. The PAR sensor was oriented toward the sky approximately 2 cm above a representative leaf from each
51 species (PARsky). The measurement was then repeated with the PAR sensor oriented
downward and approximately 5 cm above the sand substrate (PARsand).
Stomatal Frequency and Distribution
One fully expanded leaf located on the third to fifth branch of six representative
individuals of each species was collected on 18 June 2003, 20 July 2003, 19 May 2004,
18 June 2004 and 18 June 2008, stored in a cooler and transported to the laboratory for determination of adaxial and abaxial stomatal frequencies. An epidermal peel of both the adaxial and abaxial surface was made following the protocol of Brewer and Smith
(1994). Stomatal counts were conducted on three distinct areas of the six different leaves
per side per species per sample date. A single factor ANOVA was used to test for within
species stomatal frequency differences due to sampling date. A Paired Student’s t-test
was used to determine significant differences between the adaxial and abaxial stomatal
means.
Internal Leaf Anatomy
One fully expanded leaf located on the third to fifth branch of five representative
individuals of each species was collected on 18 June 2008, stored in a cooler and
transported to the laboratory. Leaves were sectioned perpendicular to the midvein with a
vibratome (Smith et al. 1998, Ruzin 1999) and observed using a Zeiss Axioplan upright
light microscope (Carl Zeiss Incorporated, Germany) with a 4X objective (1:1 ratio).
Images were captured with a microscope mounted Hamamatsu color chilled 3CCD
camera (Hamamatsu Global, Japan) and analyzed using Image Pro-Plus 6.2 software
(Media Cybernetics, Bethesda, Maryland).
Photosynthetic Light Response
52 Photosynthetic light response of both the adaxial and abaxial leaf surface of each
species was measured using the Transportable Photosynthesis System (PP Systems,
Amesbury Massachusetts). The first fully expanded leaf of nine to twelve individuals of
each species was chosen for measurement. Neutral density filters were used to attenuate
natural light resulting in PAR values ranging from 2000 μmol m-2 s-1 (full sun) to 100
μmol m-2 s-1. Leaves were allowed to acclimate to new light intensities for two minutes between readings. Previous measurements have shown that leaves return to a maximum photosynthetic rate for a given PAR value within two minutes and that order of light attenuation (high to low, low to high, or random) does not affect readings. Measurements were taken on June 18, 2008 between 1245 and 1445 hours (solar time). Best-fit linear and quadratic regression equations were used to describe the relationship between PAR and photosynthesis (i.e. assimilation rate, A). Due to the quadratic relationship between
A and PAR for H. bonariensis, assimilation rates were log10 transformed (Norman and
Streiner 2000). The relationship between A and PAR for all other species was linear.
The A:PAR ratio for each leaf surface (per species) was then determined and tested for
significant differences using a single-factor ANOVA (MacDonald 2008).
Results
The Sunlight Environment
Figure III-1 shows PAR measurements of four representative sunny to partly cloudy days dispersed throughout one year. PAR values ranged from a minimum of
0 μmol m-2 s-1 to a maximum of 2200 μm m-2 s-1 for 12 August 2002, 23 March 2003 and
29 June 2003. Maximum PAR values for 26 November 2002 were 1450 μm m-2 s-1.
Passing clouds reduced instantaneous PAR by 9-72%. Measurements taken when the LI-
53 190 Quantum Sensor was oriented toward the sky (PARsky) and interfaced with the LI-
250A hand-held light meter were in general agreement with the continuous PAR
readings. Measurements taken when the LI-190 Quantum Sensor was oriented toward
the substrate (PARsand) were on average 27% of the PARsky measurements, indicating that
the albedo of the study site substrate was 0.27 (n=112, S.E. = 0.007).
Stomatal Frequency and Distribution
Adaxial stomatal frequency differences due to sampling date were not discernable
among the four species (F = 0.337, p = 0.800 for A. pumilus; F = 3.290, p = 0.073 for C.
edentula; F = 3.14, p = 0.053 for H. bonariensis and F = 1.420, p = 0.279 for I.
imbricata) therefore data were pooled and averaged to give the following results (Figure
III-2). Average adaxial and abaxial stomatal frequencies for A. pumilus were
significantly different (t = 9.290, p < 0.001) with 69 adaxial stomata mm-2 (S.E. = 3.54)
and 41 abaxial stomata mm-2 (S.E. = 5.42). This resulted in an adaxial to abaxial stomatal
frequency ratio of 1.67. Average adaxial and abaxial stomatal frequencies for C.
edentula were significantly different (t = 2.502, p = 0.028) with 130 adaxial stomata mm-
2 (S.E. = 7.94) and 110 abaxial stomata mm-2 (S.E. = 8.14). This resulted in an adaxial to
abaxial stomatal frequency ratio of 1.18. Average adaxial and abaxial stomatal
frequencies for H. bonariensis were not significantly different (t = 1.782, p = 0.087) with
130 adaxial stomata mm-2 (S.E. = 11.15) and 120 abaxial stomata mm-2 (S.E. = 7.15).
This resulted in an adaxial to abaxial stomatal frequency ratio of 1.09. Average adaxial
and abaxial stomatal frequencies for I. imbricata were not significantly different (t =
1.222, p = 0.239) with 98 adaxial stomata mm-2 (S.E. = 9.87) and 90 abaxial stomata mm-
2 (S.E. = 11.74). This resulted in an adaxial to abaxial stomatal frequency ratio of 1.09.
54 Internal Leaf Anatomy
Micrographs of A. pumilus, C. edentula, H. bonariensis and I. imbricata are presented in Figure III-3. Amaranthus pumilus leaves were bifacial with an average thickness of 511 μm (SE = 34 μm). Tissues layers included the upper epidermis
(comprising 6% of leaf thickness on average), upper mesophyll (13%), vascular tissue/bundle sheath cells (35%), lower mesophyll (37%) and lower epidermis (9%).
Amaranthus pumilus leaves oriented at a 90o angle from incident sunlight (Figure III-4).
Cakile edentula leaves were unifacial with an average thickness of 1020 μm (SE
= 71 μm). Tissue layers included the upper epidermis (4%), upper mesophyll (37%), vascular tissue/central parenchymal cells (18%), lower mesophyll (37%) and lower epidermis (4%). Cakile edentula leaves oriented at a 45o angle from incident sunlight
(Figure III-5).
Hydrocotyle bonariensis leaves were bifacial with an average thickness of 570 μm
(SE = 15 μm). Tissue layers included the upper epidermis (10%), upper mesophyll
(39%), vascular tissue/lower mesophyll (38%) and lower epidermis (13%). Hydrocotyle bonariensis leaf angle and azimuth changed daily and seasonally
(Figure III-6).
Iva imbricata leaves were unifacial with an average leaf thickness of 1699 μm
(SE = 39 μm). Tissue layers included the upper epidermis (4%), upper mesophyll (31%), vascular tissue/central parenchyma (30%), lower mesophyll (31%) and lower epidermis
(4%). Iva imbricata leaves oriented at a 45o to 90o angle from incident sunlight
(Figure III-7).
Photosynthetic Light Response
55 Adaxial and abaxial photosynthetic light response of A. pumilus leaves were
significantly different (F = 6.70, p = 0.021, Figure III-8). Although assimilation rates (A)
were similar at low light intensities (0 to approximately 600 μmol m-2 s-1), rates began to
diverge as light intensities increased. According to the equations for the best-fit line (y =
0.013x + 0.372x, r2 = 0.93 for adaxial and y = 0.008x + 0.239, r2 = 0.84 for abaxial),
adaxial assimilation rates were approximately 7 μmol m-2 s-1 higher than abaxial rates at the highest light intensities (1750 μmol m-2 s-1).
Adaxial and abaxial photosynthetic light response of C. edentula leaves were not significantly different (F = 0.988, p = 0.336, Figure III-9). According to the equations for the best-fit line (y = 0.006x + 0.562, r2 = 0.88 for adaxial and y = 0.006x – 0.004, r2 =
0.88 for abaxial), adaxial assimilation rates were less than 1 μmol m-2 s-1 higher than
abaxial rates across the entire range of light intensities.
Adaxial and abaxial photosynthetic light response of H. bonariensis leaves were
not quite significantly different (F = 0.467, p = 0.502, Figure III-10). According to the
equations for the best-fit curve (y = - 5.90 x 10-6x2 + 0.015x + 0.394, r2 = 0.70 for adaxial
and y = - 5.22 x 10-6x2 + 0.014x – 0.023, r2 = 0.81 for abaxial), adaxial assimilation rates were less than 1 μmol m-2 s-1 higher than abaxial rates at low light intensities (0 to
approximately 600 μmol m-2 s-1) and 2 μmol m-2 s-1 higher at light intensities between
600 and 1900 μmol m-2 s-1.
Adaxial and abaxial photosynthetic light response of I. imbricata leaves were not
significantly different (F = 0.147, p = 0.705, Figure III-11). According to the equations
for the best-fit line (y = 0.008x + 0.077, r2 = 0.84 for adaxial and y = 0.006x + 1.37, r2 =
0.76 for abaxial), assimilation rates were equal at low to medium light intensities (0 to
56 approximately 1000 μmol m-2 s-1). Adaxial rates were approximately 4 μmol m-2 s-1 greater than abaxial rates at the highest light intensities (1700 μmol m-2 s-1).
Discussion
The Sunlight Environment
Sunlight environment measurements presented here are in general agreement with data reported from other studies of sandy beach sites (Ehrenfeld 1990 and references therein, Greaver and Herbert 2004). While many authors have focused on measurements
-2 -1 -2 -1 of PARsky, reporting values ranging from 200 μmol m s to 2000 μmol m s
depending upon cloud cover (DeJong 1978, Barbour et al. 1985, Ishikawa et al. 1995),
only Greaver and Herbert (2004) have specifically recorded PARsand values. Their study
site was located on the sand dunes of Key Biscayne, FL. They reported albedo values of
0.20 to 0.30 depending upon microsite differences within the dunes. These values are in
close agreement with the average albedo of 0.27 for Topsail Island. In the study by
Greaver and Herbert (2004), vegetational cover greatly affected the amount of reflected
light. The authors stated that light was a spatially heterogenous resource on sand dunes.
Amaranthus pumilus
Both stomatal frequency and leaf anatomy measurements confirm that A. pumilus leaves sampled from Topsail Island were bifacial (Figures III-2 and III-4). The adaxial:abaxial stomatal frequency ratio was 1.67 (Figure III-2) with the upper epidermal and upper mesophyll layers comprising 19% of total leaf thickness (Figure III-4). Lower epidermal and mesophyll layers comprised 46% of total leaf thickness (Figure III-4).
Additionally, Kranz anatomy (bundle sheath cells) was very apparent providing evidence that A. pumilus is a C4 plant (Larcher 1995, Lambers et al. 1998). Chlorophyll containing
57 cells were only present in the bundle sheath and adjacent layers. Adaxial photosynthetic
light response of A. pumilus leaves was significantly higher than abaxial photosynthetic
light response with values similar at low PAR levels but divergent at higher levels
(Figure III-8).
These data taken together demonstrate that A. pumilus leaves sampled from
Topsail Island process adaxial and abaxial light differently. This difference makes
intuitive sense because light experienced by the abaxial surface is at least reduced by
73% from that experienced by the adaxial surface. Light may be further reduced on the
abaxial surface due to the prostrate growth form of A. pumilus with leaves oriented at a
90o angle from incident sunlight. Greaver and Herbert (2004) reached similar conclusions while studying Ipomoea pes-caprae on the sand dunes of Florida. They reported that adaxial and abaxial differences in stomatal frequency, leaf anatomy and photosynthetic light response were a direct result of differences in PARsky versus
PARsand. Additionally, whether I. pes-caprae grows over an open sand dune environment
or one with significant vegetative cover can influence abaxial leaf anatomy and
physiology due to differences in light attenuation (albedo).
Cakile edentula
Stomatal frequency data would seem to indicate that C. edentula leaves sampled
from Topsail Island are bifacial (Figure III-2). The adaxial:abaxial stomatal frequency
ratio was 1.18 which is much lower than the ratio for A. pumilus but still indicate a
significant adaxial:abaxial difference. Leaf anatomy, however, provides evidence that C.
edentula leaves are unifacial (Figure III-5). The upper epidermal and upper mesophyll
layers comprised 41% of total leaf thickness with the lower epidermal and lower
58 mesophyll layers also comprising 41% of total leaf thickness (Figure III-5). Vascular
tissue was surrounded by parenchymal cells and taken together composed 18% of total
leaf thickness (Figure III-5). Chlorophyll containing cells were present in the upper and
lower mesophyll layers. These measurements provide evidence that C. edentula is a C3 plant as previously documented (Radford et al. 1968). Adaxial and abaxial photosynthetic light response of C. edentula leaves were very similar at all light intensities (Figure III-9).
Overall these data support the idea that C. edentula leaves sampled from Topsail
Island process adaxial and abaxial light in a similar fashion. Unlike A. pumilus, C. edentula displays an upright growth form with leaves oriented at a 45o from incident
sunlight. DeLucia et al. (1991) determined that photosynthetic symmetry was related to
leaf orientation for several species found in both open and closed (understory) habitats of
the mid-western United States. Vertically oriented leaves maintained equal
photosynthetic rates when illuminated on the adaxial and abaxial surfaces while adaxial
photosynthetic rates were significantly higher than abaxial rates for horizontally oriented
leaves. DeLucia et al (1991) continue by stating that vertical leaf orientation may be
adaptive in that it can increase daily photosynthetic carbon gain for the whole leaf and
hence the plant.
Hydrocotyle bonariensis
An adaxial:abaxial stomatal frequency ratio of 1.09 suggests that H. bonarensis
leaves sampled from Topsail Island are unifacial (Figure III-2). Leaf anatomy
measurements, however, depict some asymmetry (Figure III-6). The upper epidermis
consisted of a single cell layer and accounted for 10% of total leaf thickness while the
59 lower epidermis consisted of two cell layers and accounted for 13% of total leaf
thickness. The upper mesophyll contained oval shaped cells and contributed 39% of total leaf thickness while the lower mesophyll contained spherical cells and contributed 38% of total leaf thickness. Chloroplast containing cells were located in the upper and lower mesophyll. These measurements provide evidence that H. bonariensis is a C3 plant as
previously documented (Radford et al. 1968). Adaxial and abaxial photosynthetic light
response of H. bonariensis leaves were similar at all light intensities (Figure III-10).
These data support the conclusion that H. bonariensis leaves sampled from
Topsail Island process adaxial and abaxial light in a similar fashion, but perhaps not
identical fashion. Within the setting of this study, H. bonariensis is unique in that it
grows via rhizomes with only the leaf and petiole emerging above ground. Joesting et al.
(2009) have documented that H. bonariensis leaves demonstrate a complex pattern of leaf orientation to incident sunlight that is regulated on a daily and/or seasonal timeframe.
Additionally, H. bonariensis exhibits an enormous amount of phenotypic plasticity in shoot, root and leaf structure as well as physiology (Longstreth et al. 1981, Evans and
Whitney 1992, Evans and Cain 1995). The average leaf area and petiole length of H.
bonariensis leaves growing on the foredune of Topsail Island were 10.80 cm2 (S.E. =
0.63 cm2, n = 17) and 1.86 cm (S.E. = 0.16 cm, n = 17) as compared with 33.97 cm2 (S.E.
= 2.06 cm2, n = 17) and 19.18 cm (S.E. = 1.92 cm, n = 17) for leaves growing in swales
behind the primary dune (personal observation). Longstreth et al. (1981) found that
plants grown under low PAR conditions had maximal photosynthetic rates of 20 μmol m-
2 s-1 while plants grown under high PAR conditions had maximal photosynthetic rates of
30 μmol m-2 s-1. The present study is the first to combine observations of stomatal
60 frequency, internal leaf anatomy and photosynthetic light response of H. bonariensis
leaves. It appears that H. bonariensis has the ability to utilize light efficiently on either
leaf surface. Stomatal frequency data support this idea. Although there are slight internal
anatomy asymmetries within the leaf, they apparently are so small as to not differentially
affect function.
Iva imbricata
Both stomatal frequency and leaf anatomy measurements confirm that I. imbricata leaves sampled from Topsail Island were unifacial (Figures III-2 and III-7).
The adaxial:abaxial stomatal frequency ratio was 1.09 (Figure III-2) suggesting an essentially equal distribution of stomata on the upper and lower leaf surfaces. Iva imbricata leaf anatomy was very unique and somewhat unusual (Figure III-7). The upper epidermis and upper mesophyll comprised 35% of total leaf thickness with the lower epidermis and lower mesophyll also comprising 35% of leaf thickness. Chlorophyll containing cells were found in alternating bands (three cells thick) with non-chlorophyll containing bands (one cell thick). The vascular tissue was surrounded by parenchymal cells that were present in the center of each cross section. These measurements demonstrate that I. imbricata leaves are very symmetrical (Figure III-7). As would be predicted from the stomatal frequency and leaf anatomy data, adaxial and abaxial photosynthetic light response of I. imbricata leaves were similar (Figure III-11).
These data suggest that I. imbricata leaves sampled from Topsail Island process adaxial and abaxial light in a similar manner. Iva imbricata displays an upright growth form with leaves orienting at a 45o to 90o angle from incident sunlight. Within the setting of this study, I. imbricata is unique in that it is capable of becoming a woody perennial if
61 individuals survive into successive years. First year plants growing in the foredune
habitat were used in this study but even at an early age these plants displayed a growth
habit and leaf orientation that provided substantial illumination to both leaf surfaces. Day
et al. (1990) reported a similar relationship between growth form, leaf orientation and irradiance levels when studying three subalpine species found in the Rocky Mountains
(USA). Much like the results presented here for I. imbricata, Poulson and DeLucia
(1993) determined that species with vertically oriented leaves have similar adaxial and
abaxial photosynthetic light responses while Boardman et al. (1991) concluded that a
tendency toward amphistomaty occurs in response to increased irradiance.
Applicability of leaf form/function model to BI beach plants
Amaranthus pumilus, C. edentula, H. bonariensis and I. imbricata fit the leaf form and function model proposed by Smith et al. (1997) in some respects but not in others. As predicted for a high light environment, stomata were present on both adaxial and abaxial surfaces. The number of stomata mm-2 for H. bonariensis and I. imbricata
were statistically the same while the number of adaxial stomata mm-2 were slightly higher
than the number of abaxial stomata mm-2 for C. edentula (Figure III-2). The number of
adaxial stomata mm-2 were higher than the number of abaxial stomata mm-2 for A.
pumilus (Figure III-2). This is somewhat surprising given that most amphisomatous
species have lower numbers of adaxial stomata than abaxial stomata (Larcher 1995).
Internal leaf anatomy of C. edentula and I. imbricata fit well with the proposed
model in that leaves of both species were symmetrical with multiple layers of cells
producing adaxial and abaxial palisade mesophyll (Figures III-5 and III-7). Additionally,
C. edentula leaves oriented at a 45o angle from incident sunlight while I. imbricata leaves
62 oriented at a 45o to 90o angle from incident sunlight. According to the model, the leaf anatomy and orientation displayed by C. edentula and I. imbricata predict that these plants should be found in a stressful environment although not the most stressful environment. Smith et al. (1997) state that such an environment may be very stressful when considering some abiotic factors (e.g. sunlight), but not as stressful when considering others (e.g. water limitations). Chapter IV of this dissertation examines the dynamic relationship between water availability and BI beach plant physiology and life history traits.
Leaf anatomy and orientation of A. pumilus does not completely fit the model in that the leaf is bifacial (Figure III-4) and oriented at a 90o angle from incident sunlight.
Perhaps the prostrate growth form of A. pumilus provides substantial abaxial shading
thereby affecting leaf anatomy. Additionally, A. pumilus is somewhat succulent (as are
C. edentula, H. bonariensis and I. imbricata) which is considered to be an adaptation to
high light environments (Nobel 1999). Hydrocotyle bonariensis is enigmatic in that leaf
anatomy is slightly asymmetrical (Figure III-6) and leaf orientation can change daily and seasonally (Joesting et al. 2009). Preliminary data from H.M. Joesting suggest that H.
bonariensis leaf anatomy, adaxial and abaxial stomatal frequency and leaf orientation
change in response to microenvironmental gradients found across BI beach habitats (from
foredune to swale).
Plant characteristics (i.e. leaf anatomy and orientation) are under selective
pressure to maximize photosynthesis given developmental, structural and energy
constraints (Smith and Hughes 2009). In the dessert environment of the southwestern
United States, Nobel et al. (1975) discovered that high photosynthetic rates of
63 Plectranthus parviflorus were the direct result of thicker leaves. The increased thickness
of these leaves increased mesophyll surface area and hence CO2 absorption leading to
greater rates of assimilation (A). This study was one of the first to find a direct
relationship between leaf structure and photosynthesis.
One method to evaluate plant success in a given environment is to determine
photosynthetic carbon gain (Mott et al. 1982, Pearcy et al. 1987, Chapin et al. 1987,
Poulson and DeLucia 1993, Smith et al. 1998, Nilsen et al. 2009, Smith and Hughes
2009), although other factors such as respiration rate and allocation patterns must be
considered (Salisbury and Ross 1992, Larcher 1995, Lambers et al. 1998, Barbour et al.
1999). Chapter V of this dissertation addresses limitations to photosynthetic carbon gain,
plant response and species fitness in A. pumilus, C. edentula, H. bonariensis and I.
imbricata.
In conclusion, the leaf form of A. pumilus, C. edentula, H. bonariensis and I.
imbricata generally fit model predictions for a stressful environment (Smith et al. 1997).
Other studies have suggested similar leaf form for similar environmental conditions
(Mott et al. 1982, Poulson and DeLucia 1993, Smith et al. 1998).
Literature Cited
Barbour, M.G., T.M. DeJong and B.M. Pavlik. 1985. Marine beach and dune plant communities in B.F. Chabot and H.A. Mooney [editors], Physiological Ecology of North American Plant Communities. Pages 296-322. Chapman and Hall, New York, New York (USA).
Barbour, M.G., J.H. Burk, W.D. Pitts, F.S. Gilliam and M.W. Schwartz. 1999. Terrestrial Plant Ecology (3rd edition). Benjamin Cummings Publishers, Menlo Park, CA (USA).
Barbour, M.G. and J.E. Rodman. 1970. Saga of the West Coast sea-rockets: Cakile edentula ssp. californica and C. maritima. Rhodora. 72:370-386.
64 Boardman, J.F., T.C. Vogelmann and G. Martin. 1991. Measurement of chlorophyll fluorescence within leaves using a fibreoptic microprobe. Plant, Cell and Environment. 14:719-725.
Boyd, R.S. and M.G. Barbour. 1986. Relative salt tolerance of Cakile edentula (Brassicaceae) from lacustrine and marine beaches. American Journal of Botany. 73:236-241.
Brewer, C. A. and W.K. Smith. 1994. Influence of simulated dewfall on photosynthesis and yield in soybean isolines (Glycine max) with different trichome densities. International Journal of Plant Science. 155:460-466.
Brodersen, C.R. and T.C. Vogelmann. 2007. Do epidermal lens cells facilitate the absorption of diffuse light? American Journal of Botany. 94:1061-1066.
Brodersen, C.R., T.C. Vogelmann, W.E. Williams and H.L. Gorton. 2008. A new paradigm in leaf-level photosynthesis: direct and diffuse light are not equal. Plant, Cell and Environment. 31:159-164.
Chapin, F.S., A.J. Bloom, C.B. Field and R.H. Waring. 1987. Plant response to multiple environmental factors. Bioscience 37:49-57.
Cody, M.L. and T.W.D. Cody. 2004. Morphology and spatial distribution of alien searockets (Cakile ssp.) on South Australian and Western Canadian beaches. Australian Journal of Botany. 52:175-183.
Crawford, R.M.M. 2008. Plants at the Margin. Cambridge University Press, Cambridge (GBR).
Day, T.A., E.H. DeLucia and W.K. Smith. 1990. Dorsiventrality of the photosynthetic light response in naturally occurring C3 dicots. Current Research in Photosynthesis. 4:883-886.
DeJong, T.M. 1978. Comparative gas exchange of four California beach taxa. Oecologia. 34:343-351.
DeLucia, E.H., H.D. Shenoi, S.L. Naidu and T.A. Day. 1991. Photosynthetic symmetry of sun and shade leaves of different orientations. Oecologia. 87:51-57.
Ehrenfeld, J.G. 1990. Dynamics and processes of barrier island vegetation. Aquatic Sciences. 2:437-480.
Esau, K. 1972. Anatomia vegetal. Omega Publishers, Barcelona (ESP).
Evans, J.P. 1992. The effect of local resource availability and clonal integration on
65 ramet functional morphology in Hydrocotyle bonariensis. Oecologia. 89:265- 276.
Evans, J.P. and M.L. Cain. 1995. A spatially explicit test of foraging behavior in a clonal plant. Ecology. 76:1147-1155.
Evans, J.P. and S. Whitney. 1992. Clonal integration across a salt marsh gradient by a nonhalophyte, Hydrocotyle bonariensis (Apiaceae). American Journal of Botany. 79:1344-1347.
Evans, J.R. 1995. Carbon fixation profiles do reflect light absorption profiles in leaves. Australian Journal of Plant Physiology. 22:865-873.
Evans, J.R. 1999. Leaf anatomy enables more equal access to light and CO2 between chloroplasts. New Phytologist. 143:93-104.
Evans, J.R. and T.C. Vogelmann. 2003. Profiles of 14C fixation through spinach leaves in relation to light absorption and photosynthetic capacity. Plant, Cell and Environment. 26:547-560.
Evans, J.R. and T.C. Vogelmann. 2006. Photosynthesis within isobilateral Eucalyptus pauciflora leaves. New Phytologist. 171:771-782.
Frankenberg, D. 1997. The Nature of North Carolina’s Southern Coast. The University of North Carolina Press, Chapel Hill, NC (USA).
Greaver, T.L. and T.J. Herbert. 2004. Heterogenous reflected light influences asymmetry in leaf anatomy and gas exchange. American Journal of Botany. 91:1998-2003.
Han, T., T. Vogelmann and J. Nishio. 1999. Profiles of photosynthetic oxygen-evolution within leaves of Spinacia oleracea. New Phytologist. 143:83-92.
Ishikawa, S., S. Furukawa and T. Oikawa. 1995. Zonal plant distribution and edaphic and micrometeorological conditions on a coastal sand dune. Ecological Research. 10:259-266.
Joesting, H.M., M.O. Sprague and W.K. Smith. 2009. Daily and seasonal variation in leaf orientation for the sand dune herb Hydrocotyle bonariensis. American Journal of Botany (in review).
Johnson, D.M. and W.K. Smith. 2006. Low clouds and cloud immersion enhance photosynthesis in understory species of a southern Appalachian spruce-fir forest (USA). American Journal of Botany. 93:1625-1632.
Lambers, H., E.S. Chapin III and T.L. Pons. 1998. Plant Physiological Ecology.
66 Springer Publishers, New York, NY (USA).
Larcher, W. 1995. Physiological Plant Ecology (3rd edition). Springer, Berlin (DEU).
Levitt, J. 1980. Responses of plants to environmental stresses. Volume 2. Academic Press, New York, NY (USA).
Longstreth, D.J., T.L. Hartsock and P.S. Nobel. 1981. Light effects on the development and photosynthetic capacity of Hydrocotyle bonariensis Lamark. Photosynthetic Research. 2:95-104.
MacDonald, J. H. 2008. Handbook of Biological Statistics. Sparky House Publishing, New York, NY (USA).
Mooney, H.A. and G.L. Gulmon. 1979. Environmental and evolutionary constraints on the photosynthetic characteristics of higher plants in T. Solbrig, S. Jain, G.B. Johnson and P.H. Raven [editors], Topics in Plant Population Biology. Pages 316-337. Columbia University Press, New York, NY (USA).
Moss, D.N. 1964. Optimum lighting of leaves. Crop Science. 4:131-136.
Mott, K.A., A.C. Gibson and J.W. O’Leary. 1982. The adaptive significance of amphistomatic leaves. Plant, Cell and Environment. 5:455:460.
Nilsen, E.T., T.T. Lei and S.W Semones. 2009. Presence of understory shrubs contrains carbon gain in sunflecks by advance-regeneration seedlings: evidence from Quercus rubra seedlings grown in understory forest patches with or without evergreen shrubs present. International Journal of Plant Science. 170:735-747.
Nobel, P.S. 1999. Physiochemical and environmental plant physiology (2nd edition). Academic Press, New York, NY (USA).
Nobel, P.S., L.J. Zaragoza and W.K. Smith. 1975. Relation between mesophyll surface area, photosynthetic rate, and illumination level during development for leaves of Plectranthus parviflorus Henckel. Plant Physiology. 55:1067-1070.
Norman, G.R.N. and D.L. Streiner. 2000. Biostatistics: the bare essentials. B.C. Decker Publishers, London (GRB).
Oguchi, R., K. Hikosaka and T. Hirose. 2003. Does the photosynthetic light-acclimation need change in leaf anatomy? Plant, Cell and Environment. 26:505-512.
Oya, V.M. and A.K. Laisk. 1975. Adaptation of the photosynthetic apparatus to the light profile in a leaf. Fiziologiya Rastenii. 23:445-451.
Parkhurst, D.F. 1978. the adaptive significance of stomatal occurrence on one or both
67 surfaces of leaves. Journal of Ecology. 66:367-383.
Pearcy, R.W., O. Bjorkman, M.M. Caldwell, J.E. Keeley, R.K. Monson and B.R. Strain. 1987. Carbon gain by plants in natural environments. Bioscience. 37:21-29.
Poulson, M.E. and E.H. DeLucia. 1993. Photosynthetic and structural acclimation to light direction in vertical leaves of Silphium terebinthinaceum. Oecologia. 95:393-400.
Proietti, P. and A. Palliotti. 1997. Contribution of the adaxial and abaxial surfaces of olive leaves to photosynthesis. Photosynthetica. 33:63-69.
Radford, A.E., H.E. Ahles and C.R. Bell. 1968. Manual of the Vascular Flora of the Carolinas. The University of North Carolina Press. Chapel Hill, North Carolina (USA).
Rocas, G. and F.R. Scarano. 2001. Leaf anatomical variation in Alchornea triplinervia (Spreng) Mull. Arg. (Euphorbiacaea) under distinct light and soil water regimes. Botanical Journal of the Linnaean Society. 136:231-238.
Ruzin, S.E. 1999. Plant Microtechnique and Microscopy. Oxford University Press. 322 pages.
Salisbury, F.B. and C.W. Ross. 1992. Plant Physiology (4th edition). Wadsworth Publishing Company, Belmont, CA (USA).
Shao, G., H.H. Shugart and B.P. Hayden. 1996. Functional classifications of coastal barrier island vegetation. Journal of Vegetation Science. 7:391-396.
Soares, A.S., S.P. Dricoll, E. Olmos, J. Harbinson, M.C. Arrabaca and C.H. Foyer. 2007. Adaxial/abaxial specification in the regulation of photosynthesis and stomatal opening with respect to light orientation and growth with CO2 enrichment in the C4 species Paspalum dilatatum. New Phytologist. 177:186-198.
Smith, W.K., D.T. Bell and K.A. Shepherd. 1998. Associations between leaf structure, orientation, and sunlight exposure in five western Australian communities. American Journal of Botany. 85:56-63.
Smith, W.K. and N.M. Hughes. 2009. Progress in coupling plant form and photosynthetic function. Castanea. 74:1-26.
Smith, W.K., T.C. Vogelmann, E.H. DeLucia, D.T. Bell and K.A. Shepherd. 1997. Leaf form and photosynthesis. Bioscience. 47:785-793.
Stallman, D.A. 2004. Echoes of Topsail. Carlisle Printing, Sugarcreek, OH (USA).
68 Sun, J. and J.N. Nishio. 2001. Why abaxial illumination limits photosynthetic carbon fixation in spinach leaves. Plant Cell Physiology. 42:1-8.
Terashima, I. 1986. Dorsiventrality in photosynthetic light response curves of a leaf. Journal of Experimental Botany. 37:399-405.
United States Fish and Wildlife Service. 1993. Endangered and threatened wildlife and plants; Amranthus pumilus (seabeach amaranth) determined to be threatened. Federal Register 58(65):18035-18041.
Wang, Y., K. Noguchi and I. Terashima. 2008. Distinct light responses of the adaxial and abaxial stomata in intact leaves of Helianthus annuus L. Plant, Cell and Environment. 31:1307-1316.
Weakley, A.S. and M.A. Bucher. 1992. Status survey of seabeach amaranth (Amaranthus pumilus Rafinesque) in North and South Carolina. Report to the North Carolina Plant Conservation Program and Endangered Species Field Office, North Carolina (USA).
Woodward, F.I., J.A. Lake and W.P. Quick. 2002. Stomatal development and CO2: ecological consequences. New Phytologist. 153:477-484.
Yano, S. and I. Terashima. 2001. Separate localization of light signal perception for sun or shade type chloroplast and palisade differentiation in Chenopodium album. Plant and Cell Physiology. 42:1303-1310.
Yano, S. and I. Terashima. 2004. Developmental processes of sun and shade leaves in Chenopodium album L. Plant, Cell and Environment. 27:781-793.
69 cloud cover
2500
2000
150 0 12 August 2002 10 0 0
500
0 48121620 SOLAR TIME (hrs X 100)
2500
2000 cloud cover 15 0 0 26 November 2002 1000
500
0 4 8 12 16 2 0 SOLAR TIM E (hrs X 100)
2500 cloud cover 2000
150 0 23 March 2003 10 0 0
500
0 48121620 SOLAR TIME (hrs X 100)
2500
2000 ) -1
s cloud cover -2 1500 29 June 2003 mol m mol
1000
PAR ( PAR 500
0 4 8 12 16 20 SOLAR TIME (hrs X 100)
Figure III-1. Photosynthetically Active Radiation (PAR) measurements taken on representative days during 2002 and 2003.
70
160 1.18 * 1.09 140 Adaxial Abaxial 120 1.09
100 ) -2 80 1.67* (mm 60
40 STOMATAL FREQUENCY
20
0 A. pumilus C. edentula H. bonariensis I. imbricata
SPECIES
Figure III-2. Average adaxial and abaxial stomatal frequencies of four species of North
Carolina (USA) barrier island beach plants. Stomatal counts were made on three distinct
areas of six different leaves per side per species per sample date. Sample dates were
28 June 2003, 20 July 2003, 19 May 2004, 18 June 2004 and 18 June 2008. Bars
represent standard error. The number above each histogram is the adaxial:abaxial
stomatal ratio. Asterisks denote significant differences between adaxial and abaxial frequencies.
71
A B
C D
scale bar (150 μm for A and B, 300 μm for C and D)
Figure III-3. Transverse leaf cross sections of (A) Amaranthus pumilus, (B) Cakile edentula, (C) Hydrocotyle bonariensis and (D) Iva imbricata. Leaves were sectioned perpendicular to the midvein with a vibratome and observed using a Zeiss Axioplan upright light microscope (Carl Zeiss Incorporated, Germany). Images were captured with a microscope mounted Hamamatsu color chilled 3CCD camera (Hamamatsu Global, Japan).
72
incident sunlight
6% upper epidermis 30 μm (SE 8 μm)
13% upper mesophyll 66 μm (SE 3 μm)
vascular tissue 172 μm (SE 3 μm) 35% bundle sheath 511 μm (SE 34 μm) cells
37% lower mesophyll 197 μm (SE 17 μm)
9% lower epidermis 46 μm (SE 5 μm) 100%
reflected sunlight
Figure III-4 . Schematic cross section of an Amaranthus pumilus leaf. Chloroplast containing cells are indicated by shading. Five representative sections from five leaves were taken to obtain measurements. Leaves orient at a 90o angle from incident sunlight.
73 incident sunlight
4% upper epidermis 43 μm (SE 7 μm)
upper mesophyll 37% 381 μm (SE 43 μm)
vascular tissue 18% central 186 μm (SE 22 μm) 1020 μm parenchyma (SE 71 μm)
37% lower mesophyll 377 μm (SE 45 μm)
4% lower epidermis 33 μm (SE 1 μm)
100% reflected sunlight
Figure III-5 . Schematic cross section of a Cakile edentula leaf. Chlorophyll containing cells are indicated by shading. Five representative sections from five leaves were taken to obtain measurements. Leaves orient at a 45o angle from incident sunlight.
74 incident sunlight
10% upper epidermis 56 μm (SE 9 μm)
39% upper mesophyll 222 μm (SE 10 μm)
570 μm (SE 15 μm) vascular tissue 38% lower mesophyll 218 μm (SE 9 μm)
13% lower epidermis 75 μm (SE 9 μm) 100%
reflected sunlight
Figure III-6 . Schematic cross section of a Hydrocotyle bonariensis leaf. Chlorophyll containing cells are indicated by shading. Five representative sections from five leaves were taken to obtain measurements. Leaf angle and azimuth can change daily and seasonally. In this representation, the leaf is oriented at a 90o angle from incident sunlight.
75
incident sunlight
4% upper epidermis 63 μm (SE 4 μm)
31% upper mesophyll 535 μm (SE 22 μm)
vascular tissue 30% central parenchyma 505 μm (21 SE μm) 1699 μm (SE 39 μm)
533 μm (SE 19 μm) 31% lower mesophyll
4% lower epidermis 62 μm (SE 3 μm) 100%
reflected sunlight
Figure III-7 . Schematic cross section of an Iva imbricata leaf. Chlorophyll containing cells are indicated by shading. Five representative sections from five leaves were taken to obtain measurements. Leaves orient at a 45o to 90o angle from incident sunlight. In this representation, the leaf is oriented at a 90o from incident sunlight.
76
30 adaxial surface, y = 0.013x + 0.0372, r2 = 0.93, p<0.001 abaxial surface, y = 0.008x + 0.0239, r2 = 0.84, p<0.001 25 ) 1 - 20 s 2 - m 2 15 mol CO
10 A (
5
0 0 200 400 600 800 1000 1200 1400 1600 1800 2000 PAR (mol m-2 s-1)
Figure III-8. Photosynthetic light response of Amaranthus pumilus leaves (n = 9) illuminated on the adaxial and abaxial leaf surfaces were significantly different (F = 6.70, p = 0.021). Equations located in the figure legend describe the best-fit line for each data set (adaxial and abaxial). Measurements were taken on 18 June 2008 between 1245 and 1445 hours, solar time.
77
30
adaxial surface, y = 0.006x + 0.562x, r2 = 0.88, p<0.001 2 25 abaxial surface, y = 0.005x - 0.004x, r = 0.88, p<0.001 ) 1 - 20 s 2 - m 2 15 mol CO
10 A (
5
0 0 200 400 600 800 1000 1200 1400 1600 1800 2000 PAR (mol m-2 s-1)
Figure III-9. Photosynthetic light response of Cakile edentula leaves (n = 11) illuminated on the adaxial and abaxial leaf surfaces were not significantly different (F = 0.988, p = 0.336). Equations located in the figure legend describe the best-fit line for each data set (adaxial and abaxial). Measurements were taken on 18 June 2008 between 1245 and 1445 hours, solar time.
78
30
adaxial surface, y = - 5.90 x 10-6x2 + 0.015x + 0.394, r2 = 0.70 -6 2 2 25 abaxial surface, y = - 5.22 x 10 x + 0.014x - 0.023, r = 0.81
) 1 - 20 s 2 - m 2 15 mol CO
10 A (
5
0 0 200 400 600 800 1000 1200 1400 1600 1800 2000 PPF (mol m-2 s-1)
Figure III-10. Photosynthetic light response of Hydrocotyle bonariensis leaves (n = 12) illuminated on the adaxial and abaxial leaf surfaces were not significantly different (F = 0.467, p = 0.5.02, assimilation data were log10 transformed prior to analysis). Equations located in the figure legend describe the best-fit curve for each data set (adaxial and abaxial). Measurements were taken on 18 June 2008 between 1245 and 1445 hours, solar time.
79
30
adaxial surface, y = 8.07 x 10-3x + 0.077, r2 = 0.84, p<0.001 abaxial surface, y = 6.69 x 10-3x + 0.669, r2 = 0.90, p<0.001 25 ) 1 - 20 s 2 - m 2 15 mol CO
10 A (
5
0 0 200 400 600 800 1000 1200 1400 1600 1800 2000
-2 -1 PAR (mol m s )
Figure III-11. Photosynthetic light response of Iva imbricata leaves (n = 11) illuminated on the adaxial and abaxial leaf surfaces were not significantly different (F = 0.147, p = 0.705). Equations located in the figure legend describe the best-fit line for each data set (adaxial and abaxial). Measurements were taken on 18 June 2008 between 1245 and 1445 hours, solar time.
80 CHAPTER IV
IMPORTANCE OF AND RESPONSE TO WATER STRESS IN BARRIER ISLAND
BEACH PLANT SPECIES
Introduction
The barrier beach has been described as an abiotically challenging and physically
controlled environment (as defined by Sanders 1968). Plant physical stressors include
high levels of irradiation, high substrate surface temperatures, sand movement, salt
aerosols, overwash due to storm surges, nutrient limitations, and low water holding
capacity of the substrate (Au 1974, Barbour et. al. 1985, Ehrenfeld 1990, Hesp 1991).
Several studies have proposed that low water availability can act as a limiting factor by
affecting distribution, growth and reproduction in barrier beach plant species (Huiskes
1977, Ashenden 1978, Payne and Maun 1984, Maun 1994, Zhang 1996). For example,
Ashenden (1978) found that drought greatly reduced the transpiration rate and growth
rate of Dactylis glomerata, a European sand dune associate. Artificial watering
treatments reversed these trends. Other studies have determined that water stress was not
a limiting factor in the barrier beach environment (Au 1974, van der Valk 1974, Tyndall
et. al. 1986, Ripley and Pammenter 2004). For example, Ripley and Pammenter (2004)
discovered that water stored in sand dunes was sufficient to meet the growth requirements of Arctotheca populifola, Ipomoea pes-caprae and Scaevola plumieri, three
South African barrier beach plant associates. Apparently a contradiction concerning the importance of water availability as a limiting factor exists in the literature.
81 Differences in microenvironment between study sites could explain some of the
conflicting results found in the literature. For example, Tyndall et al. (1986) stated that
water stress was not a limiting factor for Cakile edentula living in the driftline, but that
water stress was a limiting factor for C. edentula living on the foredunes (see Figure I-4
for a description of BI beach habitats). Keddy (1981) and Payne and Maun (1984) found
that small variations in location along transects was correlated with differential survival
of Cakile maritima. This was partially attributable to moisture differences in relation to
horizontal microsite. Any study addressing water limitations in the barrier island (BI)
beach environment needs to take microenvironmental gradients into account.
Traditionally research has focused on the total amount of rain that falls in a given
environment in relation to plant survival and reproduction (Ehrenfeld 1990, Salisbury and
Ross 1992). More recently there has been interest in the timing and pattern of rainfall
and its corresponding effects on plants as well as plant response (Cheng et al. 2006, Loik
2007, Resco et al. 2008). In a review of the literature, Schwinning et al. (2004) concluded that timing of rainfall events, threshold values and even plant “memory” of such events may be as or more important than total yearly rainfall in given ecosystems.
Although coastal rainfall data is plentiful in the literature and some seasonal patterns are apparent for given locations, few studies have documented intra-month or especially intra-day rainfall patterns or relate this data to the ecophysiology of BI beach plants
(Barbour et al. 1999).
Much attention has been given to the physiological response of plants to water
stress (Schulze et al. 1987, Osmond et al. 1987, Ackerly 2004). Plants can conserve
water by regulating stomatal opening (Nobel 1999), leaf orientation to incident sunlight
82 (Ehleringer and Werk 1986, Smith et al. 1997), internal and external leaf anatomy
(Ehleringer and Mooney 1978, Smith and Hughes 2009) and biochemical processes
(McDowell et al. 2008 and references therein). Ishikawa et al. (1990) measured the net photosynthetic and transpiration rates of three Japanese coastal dune plants and developed a conceptual framework for how they mediate water stress. The authors described each species as employing either an evading, enduring or resisting strategy.
These can be combined to fit the desiccation avoidance and tolerance categories put forth by both Larcher (1995) and Lambers et al. (1998).
Few specific investigations relating the life-history traits of barrier beach plants to mediation of water stress are available in the literature (Barbour et al. 1985, Ehrenfeld
1990) although studies do exist for other environments (Salisbury and Ross 1992, Nobel
2002, Griffith and Watson 2005). For example, desert ephemerals are a well-documented group of plants that complete their life-cycle within a very short period of time when rainfall is plentiful (Barbour et al. 1999). Similarly, in one of the few studies involving life-history traits of sand dune plants, DeJong and Klinkhamer (1988) reported that germination of Cirsium vulgare and Cynoglossum officinale was strongly correlated with
rainfall events. Studies in some environments have addressed modifications in plant life-
history strategies with respect to global climate change (Cleland et al. 2007, Freville et al.
2007, Franks and Weis 2008).
The purposes of the following study were to:
1. Categorize water availability in the barrier island (BI) beach environment of Topsail
Island, North Carolina (USA).
83 2. Address strategies for mediating water stress employed by four species representing distinct functional plant groups (as defined by Shao et al. 1996, Crawford 2008).
Materials and Methods
Study Site
Topsail Island is a low topographic relief, 42 km long BI that varies in width from
150 to 500 m located approximately 40 km northeast of Wilmington, North Carolina
(Stallman 2004). The island is extensively developed with single family homes along almost its entire length (Frankenburg 1997). The study site was located on the southwestern end of the island (34o 20’ 50” N, 77o 39’ 5” W) adjacent to New Topsail
Inlet. Due to migration of the inlet to the southwest at an average rate of 35 m per year, an extensive beach and dune environment extends approximately 1-2 km from the inlet to the first beach home.
Species
Amaranthus pumilus (Rafinesque) is a pioneering C4 annual species that inhabits the driftline and foredune area of the BI beach (Weakley and Bucher 1992). The plant has a prostrate growth form, succulent leaves and pink to reddish stems. As a result of population decline due to habitat loss, A. pumilus was listed as federally threatened in
1993 (Weakley and Bucher 1992, United States Fish and Wildlife Service 1993). Cakile edentula (Bigelow) Hooker is a pioneering C3 annual species that has an upright growth form and succulent leaves (Radford et al. 1968). The plant is common within its range
(Barbour and Rodman 1970) and unlike A. pumilus, C. edentula can persist into a second growing season in moderate climates (Barbour and Rodman 1970, Boyd and Barbour
1993, Cody and Cody 2004). Hydrocotyle bonariensis Lamarck is a C3 perennial species
84 whose seeds germinate in swales located landward of the primary dune on BI beaches
(Evans 1992a). Plants often grow seaward into the foredune via rhizomes (Evans 1992a).
Leaves are peltate, vary in width from 4 to 12 cm and senesce in winter with the rhizomes
persisting underground until the next growing season (Radford et al. 1968). Iva
imbricata Walter is a succulent leaved, woody C3 shrub that can grow to heights of 1 m
and widths of 3 m (Radford et al. 1968). As a seedling, I. imbricata coinhabits the
driftline with A. pumilus and C. edentula.
Micrometeorological Measurements
All micrometeorological measurements were made continuously from June 2002
until June 2004. Rainfall measurements were conducted using a drip-tip bucket
connected to a HOBO data logger (Onset Computer Corporation, Bourne MA). To
determine the distribution of rain within each twenty-four hour period, each day was equally divided into four time segments (0001-0559, 0600-1159, 1200-1759 and 1800-
2359 Solar Time). The average monthly rainfall within each time segment was then determined. Subsequently, average yearly rainfall within each time segment was calculated and a Chi-square test for goodness of fit was performed to determine if rainfall was equally distributed throughout the day. Photosynthetically Active Radiation (PAR) was measured using a LI-190 Quantum Sensor (Li-Cor, Lincoln Nebraska) interfaced with a HOBO data logger via a Universal Transconductance Amplifier (EME Systems,
Berkley CA). Photosynthetically Active Radiation was plotted against solar time giving
a daily PAR curve. Total daily PAR was calculated by determining the area under the
curve. Air temperature measurements were made using a HOBO H8 Pro Series data
85 logger in conjunction with a solar radiation shield (Onset Computer Corporation, Bourne
MA).
Soil Water Content
A temporary transect positioned in the driftline and running parallel to the
shoreline was established during each of four sampling periods from April to July 2004.
Approximately 100 g of sand from 10 cm, 30 cm and 50 cm depth at three locations
along the transect (0 m, 75 m and 150 m) was excavated, placed in a plastic bag, sealed
and transported to the laboratory. The next day sand samples were weighed, oven dried at 30oC for twenty-four hours and reweighed. The difference in weights was used to determine soil water content on a percent basis.
Life-History Traits
Four permanent quadrats (3 m X 3 m) were established in representative areas of
the foredune habitat and observed once per month from August 2001 until November
2004. Number of H. bonariensis leaves (genets) and reproductive structures were
counted during each observation. Condition of leaves (e.g. green – actively
photosynthesizing, brown – senescing) were noted.
One permanent belt-transect (25 m X 150 m) running parallel to the shoreline was
established in a representative area of the driftline. Observations were made once per
month from July 2004 until June 2008. Number of A. pumilus, C. edentula and I.
imbricata individuals were counted during each observation. Number of leaves for each plant was estimated and noted. Condition of plants (e.g. flowers, fruits, green leaves,
senescing) was also recorded.
Xylem Water Potential
86 Xylem water potential (Ψ) measurements were taken approximately every three
hours from dawn until dusk on 21 June 2002, 12 August 2002, 26 November 2002, 23
March 2003 and 29 June 2003. The first fully expanded leaf of five different individuals
for each species was excised and placed in a Scholander-type pressure chamber (PMS
Instruments, Corvallis OR) to determine xylem water potential () (see Scholander 1965
for details).
Gas Exchange
Gas exchange measurements were taken approximately every three hours from
dawn until dusk on 21 June 2002, 12 August 2002, 26 November 2002, 23 March 2003
and 29 June 2003. The first fully expanded leaf of five different individuals for each
species was measured using the TPS Portable Photosynthesis System (PP Systems,
Amesbury, Massachusetts). Photosynthesis (A), stomatal conductance (g) and
transpiration (E) were calculated from the CO2 flux rate.
Results
Micrometerological Measurements
Rainfall patterns from 1 July 2002 until 30 June 2003 are depicted in Figure IV-1.
Table IV-1 gives the total monthly rainfall from the same time period. October through
January was the driest period of the year with each month accounting for approximately
4% of total yearly rainfall. February, April, June, July and September experienced
moderate rain with each month accounting for approximately 8% of total yearly rainfall.
March and May accounted for 10% and 12% of total yearly rainfall, respectfully. This
was due in part to storm events that occurred during both months (Figure IV-1). A
tropical storm supplied the majority of rain over a four day period during the month of
87 August. As a result, August accounted for 22% of total yearly rainfall (Table IV-1). No
clear pattern could be discerned for the distribution of average monthly rainfall within
each time segment (Table IV-1). Average yearly rainfall occurring during each time
segment was evenly distributed (χ2 = 2.07, df = 3, p<0.001).
Figure IV-2 shows PAR measurements taken on the same days as water potential and gas exchange measurements (with the exception of 21 June 2002). Total PAR measured on 12 August 2002 was 48.76 mol m-2, total PAR measured on 26 November
2002 was 16.93 mol m-2, total PAR measured on 23 March 2003 was 46.90 mol m-2 and total PAR measured on 29 June 2003 was 63.53 mol m-2.
The maximum air temperature on 21 June 2002 was 29oC, while the minimum air
temperature was 22oC. The maximum air temperature on 12 August 2002 was 31 oC, while the minimum air temperature was 21 oC. The maximum air temperature on 26
November 2002 was 14 oC, while the minimum air temperature was 3 oC. The maximum
air temperature on 23 March 2003 was 23 oC, while the minimum air temperature was 11
oC. The maximum air temperature on 29 June 2003 was 31 oC, while the minimum air
temperature was 22 oC.
Soil Water Content
Table IV-2 depicts soil water content measurements taken at different depths on
19 April, 19 May, 18 June and 12 July 2004. At 10 cm depth, soil water content ranged
from 1.29% to 3.47% with an average of 2.81% for all measurement periods. At 30 cm
depth, soil water content ranged from 2.72% to 3.73% with an average of 3.18% for all
measurement periods. At 50 cm depth, soil water content ranged from 3.69% to 3.97%
with an average of 3.83% for all measurement periods (Table IV-2). There was 0.15 to
88 0.18 cm of precipitation one day before the 19 April, 19 May and 18 June measurements.
There was 0.81 cm of precipitation one day before the 12 July measurement.
Life History Traits
Observations from quadrats (for H. bonariensis) and the belt-transect (for A.
pumilus, C. edentula and I. imbricata) are summarized in Figure IV-3. On Topsail
Island, A. pumilus germinates in late April or early May in association with subsurface
sand temperatures reaching 32oC and a rain event (Hancock and Hosier 2003).
Amaranthus pumilus begins flowering in July with fruits becoming mature in late
August/early September. Senescence occurs from late September to early November depending upon fall storm surge, cold temperatures and possibly day length (Weakley and Bucher 1992, Hancock and Hosier 2003). Cakile edentula continuously germinates beginning in late October/early November through June, flowering and fruiting at low levels from December through June. A large reproductive burst occurs in June and July, continuing until late July/early August when the plant senesceses. New leaves of H. bonariensis emerge from rhizomes in March. Flowering structures emerge in early June with fruits maturing by late August. Leaves senesce by late December when the rhizome becomes dormant (Evans 1988, 1991). Iva imbricata germinates in early April, flowers in July and fruits in early October. Senescence usually takes place in late December.
Xylem Water Potential
Xylem water potential (Ψ) varied with environmental conditions and species measured (Figure IV-4). On 12 August 2002 (clear day with scattered clouds, Tmax =
34oC, 0.46 cm of rain fell six days prior), A. pumilus and I. imbricata experienced a gradual decline in Ψ from -0.1 MPa to -0.3 and -0.5 MPa, respectively. Hydrocotyle
89 bonariensis demonstrated no change in Ψ. Cakile edentula had already senesced before
these measurements were taken (see Figure IV-3). On 26 November 2002 (partly cloudy
o day, Tmax = 14 C, 0.81 cm of rain fell nine days prior), Ψ of C. edentula increased during the day from -1.0 to -0.8 MPa. Iva imbricata exhibited a similar increase from -0.7 to
-0.4 MPa. Hydrocotyle bonariensis did not experience an appreciable change in Ψ.
Amaranthus pumilus had senesced before these measurements were taken (see Figure IV-
o 3). Measurements taken on 23 March 2003 (clear day with scattered clouds, Tmax = 23 C,
8.53 cm of rain fell two days prior), included only C. edentula and H. bonariensis due to the senescence of A. pumilus and I. imbricata. The Ψ of C. edentula declined from -0.7 to -1.1 MPa just after 1200 solar time and then rebounded to -0.8 MPa by the final measurement period. The Ψ of H. bonariensis did not change throughout the day. On 29
o June 2003 (clear day, Tmax = 36 C, 3.35 cm of rain fell nine days prior), A. pumilus and
C. edentula predawn Ψ measurements were -0.2 and -0.8 MPa, respectively. As the day
progressed, Ψ values for A. pumilus declined to -1.1 MPa while Ψ values for C. edentula
declinded to -1.5 MPa by 1600 solar time. Cakile edentula Ψ values returned to predawn
levels by the final measurement period, while A. pumilus Ψ values returned to just below
predawn levels. Xylem water potential of both H. bonariensis and I. imbricata declined
slightly (-0.1 MPa) around 1600 solar time.
Gas Exchange
Figure IV-5 depicts diurnal assimilation rates (A) for A. pumilus, C. edentula, H.
bonariensis and I. imbricata taken on four representative days during 2002-2003. On 12
August 2002, the assimilation rate of A. pumilus reached a maximum of 18 mol m-2 s-1 around 1000 solar time then abruptly dropped to 9 mol m-2 s-1 by the next measurement
90 period. Assimilation rate declined gradually the remainder of the day. The assimilation
rate of H. bonariensis peaked around 0830 with a value of 8 mol m-2 s-1 and remained
essentially unchanged until 1415 after which time the rate declined to 0 mol m-2 s-1 by
1830 solar time. Iva imbricata experienced a maximum assimilation rate of 14 mol m-2
s-1 by 0830. The assimilation rate declined to 10 mol m-2 s-1 by the next measurement
period then continued to decline gradually the remainder of the day. Cakile edentula was
not present during the 12 August 2002 measurement period.
Cakile edentula, H. bonariensis and I. imbricata exhibited similar assimilation rates on 26 November 2002 (Figure IV-5). The maximum assimilation value for any species on this day was 6 mol m-2 s-1. Cakile edentula was the only species present on
23 March 2003. On that day, assimilation rates for C. edentula reached a maximum
value of 10 mol m-2 s-1 by 1100 solar time, remained at the same value during the next measurement period, then began a gradual decline to 0 mol m-2 s-1 by 1800 solar time.
On 29 June 2003, the assimilation rate of A. pumilus peaked at 15 mol m-2 s-1 by
1130 solar time, with values gradually declining thereafter. Cakile edentula and I. imbricata obtained assimilation rates of approximately 14 mol m-2 s-1 and 16 mol m-2 s-
1 by 0900 solar time, respectively (Figure IV-5). Values of A for C. edentula increased to
a maximum of 16 mol m-2 s-1 by mid-afternoon, after which time they declined
gradually. The assimilation rate of I. imbricata declined to 8 mol m-2 s-1 by 1330 solar
time then continued to decline, although more gradually, thereafter. The assimilation rate
of H. bonariensis peaked at 7 mol m-2 s-1 by 0900 solar time, declined to 3 mol m-2 s-1
by 1330 solar time, increased slightly during the next measurement period, then declined
to 0 mol m-2 s-1 during the final period.
91 Figure IV-6 shows stomatal conductance rates (g) for A. pumilus, C. edentula, H.
bonariensis and I. imbricata taken on four representative days during 2002-2003. On 12
August 2002, stomatal conductance for A. pumilus increased from an initial value of 59
mmol m-2 s-1 to 100 mmol m-2 s-1 by 1030. Stomatal conductance then decreased to 58
mmol m-2 s-1 by the 1415 measurement period. Values of g remained relatively constant
for the remainder of the day. The initial stomatal conductance value for H. bonariensis
was 28 mmol m-2 s-1. Stomatal conductance increased to 66 mmol m-2 s-1 by the next
measurement period, then continued to increase but more gradually until a maximum
value of 79 mmol m-2 s-1 was reached by the 1415 solar time. Values of g decreased
relatively rapidly through the last measurement period for the day. The initial g value of
I. imbricata was 19 mmol m-2 s-1. Stomatal conductance increased to 91 mmol m-2 s-1 by the next measurement period. Values then began to decline gradually for the remainder of the day. Cakile edentula was not present during the 12 August 2002 measurement period.
Hydrocotyle bonariensis and I. imbricata exhibited similar patterns of stomatal conductance rates on 26 November 2002 (Figure IV-6), with initial values approximately
22 mmol m-2 s-1. Stomatal conductance rates increased to 66 mmol m-2 s-1 and 77 mmol m-2 s-1 by 1030 solar time for H. bonariensis and I. imbricata, respectively. Hydrocotyle
bonariensis g values then decreased to 60 mmol m-2 s-1 by the next measurement period
and 23 mmol m-2 s-1 by the final period. Iva imbricata stomatal conductance reached a
maximum of 78 mmol m-2 s-1 at 1430 solar time decreasing to 24 mmol m-2 s-1 by the final
measurement period. Amaranthus pumilus had scenesced before these measurements
were taken.
92 Cakile edentula was the only species present on 23 March 2003. The initial value
of g was 34 mmol m-2 s-1. Cakile edentula reached a maximum stomatal conductance
rate of 120 mmol m-2 s-1 at 1030 solar time and maintained this through the next measurement period. After 1250 solar time, g values declined rapidly to 35 mmol m-2 s-1.
On 29 June 2003, stomatal conductance for A. pumilus increased rapidly from an initial value of 12 mmol m-2 s-1 to 96 mmol m-2 s-1 by the second measurement period
(Figure IV-6). Stomatal conductance continued to increase, but more gradually, until a
maximum daily value of 114 mmol m-2 s-1 was reached at 1115 solar time. Afterwards,
values of g declined gradually to 24 mmol m-2 s-1 by the final measurement period. The
initial stomatal conductance for C. edentula was 49 mmol m-2 s-1 after which it reached a
maximum value of 167 mmol m-2 s-1 by 1345 solar time. Values declined rapidly to 82 mmol m-2 s-1 by the next measurement period then declined more gradually to 67 mmol
m-2 s-1 by the final measurement. The early morning pattern of stomatal conductance
values for Iva imbricata was similar to those of A. pumilus and C. edentula with an initial
value of 27 mmol m-2 s-1. Rates increased rapidly to 102 mmol m-2 s-1 by the second
measurement period. Afterward, I. imbricata experienced a decline in g to 78 mmol m-2
s-1 with values remaining relatively unchanged over the next two measurement periods.
Final g values fell to 35 mmol m-2 s-1. Stomatal conductance values of H. bonariensis were low compared to A. pumilus, C. edentula and I. imbricata. Initial and final g values for H. bonariensis were 17 mmol m-2 s-1 and 15 mmol m-2 s-1, respectively. The
maximum daily g value was 52 mmol m-2 s-1 at 0915 solar time.
Figure IV-7 documents transpiration rates (E) for A. pumilus, C. edentula, H.
bonariensis and I. imbricata taken on four representative days during 2002-2003.
93 Transpiration rate patterns for A. pumilus, H. bonariensis and I. imbricata were similar on 12 August 2002 with initial values ranging from 0.19 to 0.44 mmol m-2 s-1. By 1030 solar time, values of E were 3.07 mmol m-2 s-1, 2.61 mmol m-2 s-1 and 2.30 mmol m-2 s-1
for A. pumilus, H. bonariensis and I. imbricata, respectively. Values declined steadily to
0 mmol m-2 s-1 by the final measurement period. Cakile edentula was not present during the 12 August 2002 measurement period.
Patterns of E for C. edentula, H. bonariensis and I. imbricata were similar on 26
November 2002 with initial values of approximately 0.20 mmol m-2 s-1 (Figure IV-7).
Transpiration rate gradually increased to a maximum of 1.19 mmol m-2 s-1, 0.68 mmol m-
2 s-1 and 0.93 mmol m-2 s-1 for C. edentula, H. bonariensis and I. imbricata, respectively.
Rates declined to approximately 0.20 mmol m-2 s-1 by the final measurement period.
Cakile edentula was the only species present on 23 March 2003. The initial value
of E was 0.30 mmol m-2 s-1. Cakile edentula reached a maximum transpiration rate of
1.65 mmol m-2 s-1 at 1230 solar time. Values declined rapidly to 0.71 mmol m-2 s-1 by the
next measurement period then continued to decline, but more slowly, reaching a final value of 0.18 mmol m-2 s-1 by 1800 solar time.
Amaranthus pumilus and Cakile edentula had similar transpiration patterns on 29
June 2003 (Figure IV-7). Initial rates were 0.15 mmol m-2 s-1 and 0.50 mmol m-2 s-1 for
A. pumilus and C. edentula, respectively. Rates increased steeply to approximately 2.70 mmol m-2 s-1 by 1115 solar time and continued to increase, but more gradually, to the daily maximum of 2.90 mmol m-2 s-1 was reached by the next measurement period.
Amaranthus pumilus values declined to 0.43 mmol m-2 s-1 while C. edentula values
declined to 1.03 mmol m-2 s-1 by 1830 solar time. Transpiration rates for H. bonariensis
94 were low compared to A. pumilus, C. edentula and I. imbricata. Initial and final values
of E for H. bonariensis were 0.19 mmol m-2 s-1 and 0.22 mmol m-2 s-1, respectively.
Transpiration increased for H. bonariensis to a maximum value of 1.18 mmol m-2 s-1 by
1115 solar time, declining to 0.77 mmol m-2 s-1 by the next measurement period. Initial
and final transpiration rates of I. imbricata were similar to the other three species
measured. Iva imbricata reached a maximum transpiration rate of 2.02 mmol m-2 s-1 at
1345 solar time. This value was intermediate when compared to the other three species
measured.
Rain Event
o On 21 June 2002 (clear day with scattered clouds, Tmax = 29 C), the initial Ψ for
A. pumilus was -0.4 MPa. Amaranthus pumilus xylem water potential increased slightly to -0.24 MPa by 1100 solar time. A rain event occurred from 1430 until 1500 solar time providing 0.81 cm of rainfall (Figure IV-8). Xylem water potential of A. pumilus declined to -1.1 MPa by the next measurement period. During the final measurement, A.
pumilus Ψ had increased to its highest level of the day (-0.1 MPa). The Ψ for C.
edentula declined rapidly to -1.2 MPa by 1100 solar time from an initial value of -0.5
MPa. During the final two measurement periods, Ψ of C. edentula steadily increased to
its highest levels of the day. The initial value of Ψ for H. bonariensis was -0.1 MPa.
Values declined to -0.3 MPa by the next measurement period. Recovery to
approximately -0.1 MPa occurred after the rain event. Iva imbricata values of Ψ remained relatively constant at -0.2 MPa during the first two measurement periods, then declined to -0.5 MPa in the mid-afternoon. The Ψ of I. imbricata increased to its highest level of the day by the final measurement period.
95 On 21 June 2002, the initial assimilation rate of all four species ranged from 0.8
to 2.0 μmol m-2 s-1 (Figure IV-8). Values of A for A. pumilus reached a maximum of 17
μmol m-2 s-1 by 1300 solar time, then declined rapidly to 5.4 μmol m-2 s-1 by 1530 solar
time. The final measurement of the day for A. pumilus was 2.0 μmol m-2 s-1.
Assimilation rates for C. edentula peaked at 9.0 μmol m-2 s-1 during the third
measurement period, remained relatively constant for the next measurement period and declined to 4.0 μmol m-2 s-1 by 1815 solar time. Hydrocotyle bonariensis assimilation rates reached 8.0 μmol m-2 s-1 during the second measurement period and declined
steadily thereafter. Values of A for I. imbricata achieved a maximum rate of 13 μmol m-2
s-1 by 1115 solar time and declined steadily thereafter.
Stomatal conductance rates were similar for all four species during the first two
measurement periods (Figure IV-8). Amaranthus pumilus stomatal conductance rates
gradually declined to 53 mmol m-2 s-1 by 1530 solar time then stayed constant for the
final measurement period. Values of g for C. edentula reached a maximum of 96 mmol
m-2 s-1 by 1530 solar time, then declined rapidly to 52 mmol m-2 s-1 for the final
measurement period. Hydrocotyle bonariensis stomatal conductance peaked at 70 mmol
m-2 s-1 during the fourth measurement period while g values for I. imbricata peaked at 71 mmol m-2 s-1 during the second measurement period.
Transpiration rates of all four species were similar with the exception that A.
pumilus peaked at 1300 solar time rather than 1530 solar time and that the maximum
rates of E for A. pumilus were 0.4 mmol m-2 s-1 higher than the other species.
96 Discussion
Soil water content measured on Topsail Island, NC was 3.3% when averaged across the four measurement days, for the three measurement depths (Table IV-2). This is consistent with data taken by Au (1974) on Shackleford Bank, NC (3.0% average soil water content), van der Valk (1977) on Cape Hatteras National Seashore, NC (4.0% average soil water content) and Dubois (1977) on Sapelo Island, GA (3.5% average soil water content). Researchers generally agree that the first few centimeters of sand dries quickly after a rain, but that deeper layers (15 - 30 cm) are usually moist regardless of time between rainfalls (Kearny 1900, Au 1974, van der Valk 1977, Dubois 1977, Barbour et al. 1985). Data from Topsail Island support these earlier studies. This phenomenon has been attributed to the insulating effect of the upper layers of sand, low matrix potential of the substrate and a relatively shallow water table (Au 1974, Barbour et al.
1985, Barbour et al. 1999, Moreno-Casasola and Vazquez 1999).
On Topsail Island, the driest and coldest part of the year with the least Total PAR coincides with the dormant phases (or the stage just before dormancy) of A. pumilus, H. bonariensis and I. imbricata (Figures IV-1, IV-2, IV-3 and Table IV-1). These life- history patterns are typical of BI beach summer C4 annuals – A. pumilus - (DeJong 1978,
Barbour et al. 1985), warm weather BI beach C3 clonals – H. bonariensis - (Evans 1988,
1991) and warm weather BI beach, woody, decidous C3 species – I. imbricata - (Radford et al. 1968, Colosi and McCormick 1978, Franks 2003a and 2003b). Germination timing of A. pumilus, H. bonariensis (emergence of new leaves), I. imbricata and to an extent C. edentula correspond to a part of the year that can experience storms providing relatively large amounts of rainfall over short periods of time. Many coastal studies have
97 documented the association between germination flushes and rainfall events (DeJong
1979, Weller 1985, DeJong and Klinkhamer 1988, Ehrenfeld 1990, Hancock and Hosier
2003, Padilla and Pugnaire 2007). The life-history of C. edentula is unique in relation to
the other three BI beach associates in that the species senesces before the hottest part of
the year when total PAR levels are highest (Figure IV-1, Figure IV-2, Figure IV-3 and
Table IV-1). These life-history traits may represent adaptations to the BI beach
environment that correspond to tolerance (A. pumilus, H. bonariensis and I. imbricta) and
avoidance (C. edentula) strategies as defined by Larcher 1995 and Lambers et al 1998.
Rainfall patterns on Topsail Island were highly variable with 40% of total yearly
precipitation associated with storm systems that provided large volumes of water in a
relatively small time period (Table IV-1, Figure IV-1). Smaller, more frequent systems
occurred in March and May (19% of total yearly parcipitation) with one large system
happening in the fall (21% of total yearly parcipitation). This seems to be a typical
pattern found along the NC coast (Barnes 2001). The large amount of water input from
these storm events and their random arrival during a given twenty-four hour period,
obscured any underlying daily rainfall patterns when considering time segments (0001-
0559, 0600-1159, 1200-1759 and 1800-2359) averaged over a given month. Average
yearly rainfall occurring during each time segment was evenly distributed as stated in the
Results, suggesting that rain is no more likely to occur in the afternoon than in the early
morning, mid-morning or evening. It would be beneficial to take similar measurements
over several years to ascertain if the patterns found in this study are the norm for Topsail
Island.
98 Amaranthus pumilus experienced a gradual decline in on 12 August 2002 due
to water loss via transpiration (Figures IV-4 and IV-7), with stomatal conductance
decreasing from 100 mmol m-2 s-1 to 58 mmol m-2 s-1 during the same time period (Figure
IV-6). On 29 June 2003, the of A. pumilus declined to -1.2 MPa during the mid-
afternoon, followed by a rebound to -0.4 MPa by the next measurement period. This was
most likely due to A. pumilus closing its stomata to conserve water (Figure IV-6). On the
same day, transpiration rates similarly reached a maximum of 2.9 mmol m-2 s-1 at 1345
solar time, declining to 2.1 mmol m-2 s-1 by the next measurement period and continuing
to decline thereafter (Figure IV-7). Amaranthus pumilus consistently had some of the
highest assimilation rates of the four species measured in this study with maximum
values of 18 μmol m-2 s-1 and 15 μmol m-2 s-1 measured on 12 August 2002 and 29 June
2003, respectively (Figure IV-5). As is typical for many plants during hot, dry periods
(Larcher 1999, Nobel 1999), of A. pumilus decreased during the day. This decrease is
associated with transpiration that accompanies photosynthesis via open stomata. It is
probable that A. pumilus can maintain relatively high assimilation rates while mediating
transpiration by controlling stomatal aperature.
Cakile edentula was absent during the 12 August 2002 measurement period,
thereby avoiding a particularly hot, dry day. During the mid-afternoon on 29 June 2003,
C. edentula experienced the lowest xylem water potential recorded in this study, -1.5
MPa (Figure IV-4). Xylem water potential recovered to -0.8 MPa by the next
measurement period. Similar to A. pumilus, this was most likely due to stomatal closure
to conserve water. Stomatal conductance was recorded as 167 mmol m-2 s-1 at 1345 solar time followed by 82 mmol m-2 s-1 at 1600 solar time (Figure IV-6). Transpiration rates
99 were very similar to those experienced by A. pumilus (Figure IV-7). The intial xylem water potential for C. edentula on 26 November 2002 was -1.0 MPa. Values increased gradually to -0.8 by the end of the day (Figure IV-4). Although stomatal conductance rates were relatively high (Figure IV-6), transpiration rates remained low (Figure IV-7).
This is probably due to a low vapor pressure deficit which is not uncommon in cooler months of the year (Barbour et al. 1985). During 23 March 2003, a warm and clear day, xylem water potential declined to a daily low of -1.0 MPa in the mid-afternoon, followed by recovery to -0.8 MPa during the final measurement period. As on 29 June 2003, this was most likely due to stomatal closure to conserve water. Transpiration rates peaked when Ψ values were lowest, then declined (Figures IV-5 and IV-6). Cakile edentula assimilation rates were relatively high with maximum values of 5 μmol m-2 s-1, 10 μmol m-2 s-1 and 17 μmol m-2 s-1 for 26 November 2002, 23 March 2002 and 29 June 2003, respectively (Figure IV-5). Through a combination of life history traits, physiological response and tolerance, C. edentula is able to maintain assimilation rates that are comparable to those of A. pumilus.
Similar to A. pumilus, I. imbricata experienced a gradual decline in on 12
August 2002 due to water loss via transpiration (Figures IV-4 and IV-7). Iva imbricata, however, appeared to be more sensitive to potential water deficit, reducing its maximum value of g (recorded at 0830 solar time) more quickly than A. pumilus (Figure IV-6).
Stomatal conductance continued to decline gradually throughout the remainder of the day. As would be expected given the stomatal conductance values, maximum transpiration rates of I. imbricata were lower than those of A. pumilus, although both plants did follow a similar diurnal pattern (Figure IV-7). Maximum assimilation rates of
100 I. imbricata on 12 August 2002 were 14 μmol m-2 s-1, considerably lower than those of A.
pumilus (Figure IV-5). The intial xylem water potential for I. imbricata on 26 November
2002 was -0.7 MPa. Values increased gradually to -0.4 by the end of the day, following a
pattern that was very similar to that of C. edentula (Figure IV-4). Stomatal conductance
values for I. imbricata were similar to those recorded on 12 August 2002, but the diurnal
pattern was different with maximum values being obtained at 1030 and 1430 solar time
(Figure IV-6). Transpiration and assimilation rates were much lower than those
measured on 12 August 2002. It is likely that I. imbricata can keep stomata open with
relatively little transpiration due to the lower vapor pressure deficit present in November
on Topsail Island. The xylem water potential of I. imbricata declined to -0.2 MPa during
mid-morning and mid-afternoon on 29 June 2003 at the same time (mid-afternoon) that Ψ
of both A. pumilus and C. edentula declined precipitously (Figure IV-4). Assimilation
rates, stomatal conductance rates and transpiration rates were all lower than those of A.
pumilus or C. edentula. The difference could be due to the fact that I. imbricata has a
substantial tap root (Colosi and McCormick 1978, Franks and Peterson 2003) that may
have access to deeper and more consistent water sources than either A. pumilus or C.
edentula.
The xylem water potential of H. bonariensis remained relatively constant during
each of the measurement days, never becoming more negative than -0.3 MPa (Figure IV-
4). Hydrocotyle bonariensis has been shown to translocate water from slacks (low areas on the dunes were the water table is closer to the surface) to the leading edge of growth in
the foredunes and primary dunes (Evans 1988, Evans 1991, Evans 1992a, Evans and
Whitney 1992, Evans and Cain 1992) and is probably doing so on Topsail Island given
101 the consistly high Ψ readings. It appears that the morphology (clonal) growth pattern of
H. bonariensis affords it a ready supply of water throughout the growing season.
Assimilation of photosynthetic CO2 (A), stomatal conductance and transpiration
rates of H. bonariensis were lower than those of A. pumilus, C. edentula and I. imbricata
during almost every measurement period (Figures IV-5, IV-6 and IV-7). Assimilation
rates reached maximum values on 12 August 2002 (7 μmol m-2 s-1) and 29 June 2003 (8
μmol m-2 s-1), both very hot and dry days. Maximum values of A for 26 November 2002
were 4 μmol m-2 s-1. Stomatal conductance and transpiration rates closely mirrored
assimilation rates (Figures IV-6 and IV-7), with one notable exception. Transpiration
rates spiked (2.6 mmol m-2 s-1) at 1050 solar time on 12 August 2002 while stomatal
conductance and assimilation remained steady. Other researchers have reported similar
high values of E without a concomitant increase in A and g values when vapor pressure deficit is large (Nobel 1999, Barbour et al. 1999).
Measurements taken on 12 August 2002, 26 November 2002, 23 March 2003 and
29 June 2003 offer an example of A. pumilus, C. edentula, H. bonariensis and I. imbricata physiological behavior during representative rainless days throughout a typical year on Topsail Island, NC. The rain event that occurred during mid-afternoon on 21
June 2002, when plant water stress is often highest (Larcher 1995, Lambers et al. 1998),
provides an opportunity to observe how BI beach plant species respond to an input of
water during a critical time period (Figure IV-8).
Amaranthus pumilus experienced a substantial decrease in xylem water potential
(Ψ) just after the rain event followed by an increase above predawn levels by the next
measurement period. The xylem water potential of C. edentula reached a daily low just
102 before the rain event then quickly rebounded to predawn levels by the next measurement
period. The diurnal pattern of I. imbricata Ψ was similar to that of A. pumilus, but the
mid-afternoon decline was not as substantial. The xylem water potential pattern of H.
bonariensis was similar to C. edentula, but the mid-morning decline was not nearly as
substantial. These differences could be explained by differential response time between
the species since stomatal conductance values were similar (with the exception of C. edentula just after the rain event). Transpiration rates were comparable for each species throughout the day (with the exception of A. pumilus just before the rain event). One difficulty with the 21 June 2002 xylem water potential data set is that only four
measurements were taken throughout the day. A fairly large expanse of time (four hours)
separates data taken before and after the rain event. A measurement taken closer to the
start of the rain event may have more completely described the physiological behavior of
each species.
Amaranthus pumilus had some of the highest assimilation, stomatal conductance
and transpiration rates measured in this study. Given its prostrate growth form,
horizontal leaf orientation and internal leaf anatomy (Chapter III), A. pumilus appears to
maximize light interception and thereby photosynthesis. The growing season for A.
pumilus is only six to seven months on Topsail Island and therefore the best strategy for
this life history pattern may be to fix as much carbon as possible in the shortest amount of
time (Chapter V). The cost of this strategy could be water loss via transpiration, but this
may be mediated by stomatal control, mesophyll biochemistry (not addressed in this
study) root architecture and the occurrence of rain events. According to Maun (1994),
many coastal plant species undergo rapid root extension during the first few weeks of
103 growth. This root extension can provide the plant with a more consistent source of water
(Laing 1958, DeJong 1979, Padilla and Pugnaire 2007, Saha et al. 2008). After
germination (which correlates with rain fall events), roots of A. pumilus seedlings quickly
grow to lengths of 25-30 cm (personal observation).
There is a growing body of literature addressing the importance of precipitation
pulses to plant water and carbon balance (de Mattos et al. 2002, Xu and Li 2006, Xu et al.
2007) with several studies documenting rapid changes in A, g, E and Ψ directly after a
rain event (de Mattos et al. 2002, Cheng et al. 2006). Such rain events within the
growing season could provide needed moisture to maintain A. pumilus photosynthetic
rates at high levels. In a study of the Florida scrub ecosystem where short, intense rain
showers are common, Saha et al. (2008) found that eight species of co-occuring plants
were “equipped to survive fluctuations in soil moisture but did not posses mechanisms to
cope with persistently dry soils because persistently low soil moisture conditions rarely
occur”. The environmental conditions of this system are similar to those that exist on
North Carolina BI beaches.
As stated earlier, the CO2 assimilation and transpirational water loss of C.
edentula were comparable to those of A. pumilus, although maximum stomatal
conductance values were larger and minimum Ψ values more negative. It is possible that
C. edentula is more tolerant of water stress than A. pumilus, which might help explain why C. edentula is common throughout its considerable range while A. pumilus is listed as threatened (Maun et al. 1990, Weakely and Bucher 1992, Hancock and Hosier 2003).
The life-history pattern of C. edentula is most likely another important aspect of its adaptation to the BI beach environment. Cakile edentula is absent during some of the
104 hottest and driest months of the year (July, August and September), while alive and active during some of the cooler months (November through April). Although assimilation
rates are not as high during the cooler months, the additive effect of photosynthesizing
nine months out of the year may allow C. edentula to reach carbon gain thresholds that
are necessary for growth and reproduction (Chapter V).
In many respects, I. imbricata exhibited physiological and life history traits that
were intermediate when considering its BI beach associates. Values of A, g, E and Ψ
were never the highest or lowest of the species measured on any given day. The lowest
value of Ψ was -0.7 MPa recorded on 26 November 2002. This is well above -1.5 MPa
given as a minimum threshold for water stress in the coastal dune environment (Au 1974,
Ehrenfeld 1990, Barbour et al. 1999). Similar to C. edentula, I. imbricata has a nine
month growing season although it is centered on the warmer parts of the year (April
through December). Moderate assimilation rates spread over nine months may be a
means to achieve required carbon gain thresholds. Perhaps I. imbricata is able to avoid
water stress and maintain photosynthesis via a combination of stomatal control, root
architecture (tap rooted, woody perennial) and life-history pattern.
Hydrocotyle bonariensis displays a survival strategy that is well suited to the BI
beach environment. The species germinates in swales (Evans 1992b), taping into the
more plentiful water supply of that habitat and extending rhizomes into the primary dune and foredune beyond. Due to this consistent water supply, H. bonariensis does not
appreciably experience water stress. Assimilation rates, stomatal conductance and
transpiration rates are low, but steady throughout the growing season, which for H. bonariensis is relatively long (ten months). Leaves senesce and the species over-winters
105 via its rhizome, ready for the next growing season with its connection to water and
nutrient supplies intact.
Conclusions
Water availability in the BI beach environment may be greater than previously thought, challenging the assumption that plants living in this environment are constantly
under water stress. Amaranthus pumilus and C. edentula did experience appreciable
decreases in xylem water potential on occasion but not usually to the extent that would be considered water stressed. Alternatively, I. imbricata and especially H. bonariensis maintained xylem water potentials well above values considered stressful. Each of the species involved in this study demonstrated physiological and life-history attributes that likely maximized photosynthetic carbon gain over a given year, albeit via different combinations of traits.
Literature Cited
Akerley, D. 2004. Functional strategies of chaparral shrubs in relation to seasonal water deficit and disturbance. Ecological monographs. 74:25-44.
Ashenden, T. 1978. Drought avoidance in sand dune populations of Dactylis glomerata. Journal of Ecology. 66:943-951.
Au, S. 1974. Vegetation and ecological processes on Shackleford Bank, North Carolina. National Park Service Scientific Monograph Series. Number 6.
Barbour, M., J. Burk, W. Pitts, F. Gilliam and M. Schwartz. 1999. Terrestrial plant ecology (3rd edition). Benjamin Cummings Publishers, Menlo Park, CA (USA).
Barbour, M.G., T.M. DeJong and B.M. Pavlik. 1985. Marine beach and dune plant communities in B.F. Chabot and H.A. Mooney [editors], Physiological Ecology of North American Plant Communities. Pages 296-322. Chapman and Hall, New York, New York (USA).
Barbour, M. and J. Rodman. 1970. Saga of the west coast sea-rockets: Cakile edentula ssp. californica and C. maritima. Rhodora 72:370-386.
106 Barnes, J. 2001. North Carolina’s hurricane history (3rd edition). The University of North Carolina Press, Chapel Hill, North Carolina (USA).
Bombelli, A. and L. Gratani. 2003. Interspecific differences of leaf gas exchange and water relations of three evergreen Mediterranean shrub species. Photosynthetica. 41:619-625.
Boyd, R.S. and M.G. Barbour. 1993. Replacement of Cakile edentula by C. maritima in the strand habitat of California. The American Midland Naturalist. 130:209-228.
Chapotin, S., J. Razanameharizaka and N. Holbrook. 2006. Water relations of baobab trees (Adansonia spp. L) during the rainy season: does stem water buffer daily water deficits? Plant, cell and environment. 29:1021-1032.
Cheng, X., S. An, B. Li, J. Chen, G. Lin, y. Liu, Y. Luo and S. Liu. 2006. Summer rain pulse size and rainwater uptake by three dominant desert plants in a desertified grassland ecosystem in northwestern China. Plant Ecology. 184:1-12.
Cleland, E.E., I. Chuine, a. Menzel, H.A. Mooney and M.d. Schwartz. 2007. Shifting plant phenology in response to global change. Trends in Ecology and Evolution. 22:357-365.
Cody, M.L. and T.W.D.Cody. 2004. Morphology and spatial distribution of alien searockets (Cakile spp.) on South Australian and Western Canadian beaches. Australian Journal of Botany. 52:175-183.
Colosi, J. and H. McCormick. 1978. Population structure of Iva imbricata in five coastal dune habitats. Bulletin of the Torrey Botanical Club. 105:175-186.
Crawford, R.M.M. 2008. Plants at the margin. Cambridge University Press, Cambridge (GRB).
De Jong, T.J. and Klinkhamer. 1988. Seedling establishment of the biennials Cirsium vulgare and Cynoglossum officinale in a sand-dune area: the importance of water for differential survival and growth. Journal of Ecology. 76:393-402.
De Jong, T.M. 1978. Comparative gas exchange of four California beach taxa. Oecologia. 34:343-351.
De Jong, T.M. 1979. Water and salinity relations of California beach species. Journal of Ecology. 67:647-663. de Mattos, E.A., P.C. Lobo and C.A. Joly. 2002. Overnight rainfall inducing rapid changes in photosynthetic behavior in a cerrado woody species during a dry spell amidst the rainy season. Australian Journal of Botany. 50:241-246.
107 Dubois, S.J. 1977. Comparative ecophysiology of C3 and C4 sand dune plant species of the Georgia coast. Master’s Thesis. University of Georgia, Athens, Georgia (USA).
Ehleringer, J.R. and H.A. Mooney. 1978. Leaf hairs: effects on physiological activity and adaptive value to a desert shrub. Oecologia. 37:183-200.
Ehleringer, J.R. and K.S. Werk. 1986. Modifications of solar-radiation absorption patterns and implications for carbon gain at the leaf level in T.J. Givnish [editor], On the Economy of Plant Form and Function. Pages 57-81. Cambridge University Press, London (GBR).
Ehrenfeld, J.G. 1990. Dynamics and processes in barrier island vegetation. Aquatic Sciences. 2:437-480.
Evans, J.P. 1988. Nitrogen translocation in a clonal dune perennial, Hydrocotyle bonariensis. Oecologia. 77:64-68.
Evans, J.P. 1991. The effect of resource integration on fitness related traits in a clonal dune perennial, Hydrocotyle bonariensis. Oecologia. 86:268-276.
Evans, J.P. 1992a. The effect of local resource availability and clonal integration on ramet morphology in Hydrocotyle bonariensis. Oecologia. 89:265-276.
Evans, J.P. 1992b. Seedling establishment and genet recruitment in a population of a clonal dune perennial. Barrier isand ecology of the Mid-Atlantic coast: a symposium. Technical Report NPS/SERCAHA/NRTR-93/04. Pages 75-84.
Evans, J.P. and M.L. Cain. 1995. A spatially explicit test of foraging behavior in a clonal plant. Ecology. 76:1147-1155.
Evans, J.P. and S. Whitney. 1992. Clonal integration across a salt gradient by a nonhalophyte, Hydrocotyle bonariensis. American Journal of Botany. 79:1344- 1347.
Franks, S.J. 2003a. Competitive and facultative interactions within and between two species of coastal dune perennials. Canadian Journal of Botany. 81:330-337.
Franks, S.J. 2003b. Facilitation in multiple life-history stages: evidence for nucleated succession in coastal dunes. Canadian Journal of Botany. 81:330-337.
Franks, S.J. and C.J. Peterson. 2003. Burial disturbance leads to facilitation among coastal dune plants. Plant Ecology. 168:13-21.
Franks, S.J. and A.E. Weiss. 2008. A change in climate causes rapid evolution of multiple life-history traits and their interactions in an annual plant. Journal of
108 evolutionary biology. 21:1-14.
Frankenburg, D. 1997. The Nature of North Carolina’s Southern Coast. The University of North Carolina Press, Chapel Hill, North Carolina (USA).
Freville, H., K. McConway, M. Dodd and J. Silvertown. 2007. Prediction of extinction in plants: interaction of extrinsic threats and life-history traits. Ecology. 88:2662- 2672.
Griffith, T.M. and M.A. Watson. 2005. Stress avoidance in a common annual: reproductive timing is important for local adaptation and geographic distribution. Journal of evolutionary biology. 18:1601-1612.
Hancock, T. and P. Hosier. 2003. Ecology of the threatened species Amaranthus pumilus Rafinesque. Castanea. 68:236-244.
Hesp, P.A. 1991. Ecological processes and plant adaptations on coastal dunes. Journal of Arid Environments. 21:165-191.
Huiskes, A. 1977. The natural establishment of Ammophila arenaria from seed. Oikos. 29:133-136.
Ishikawa, S., A. Furukawa and T. Oikawa. 1995. Zonal plant distribution and edaphic and micrometerological conditions on a coastal sand dune. Ecological Research. 10:259-266.
Ishikawa, S., T. Oikawa and A. Furukawa. 1990. Photosynthetic characteristics and water use efficiency of three coastal dune plants. Ecological Research. 5:377- 391.
Kearny, T.H. 1900. The plant covering of Ocracoke Island: a study in the ecology of the North Carolina strand vegetation. United States National Herbarium, Contributions. 5:321-585.
Keddy, P. 1981. Experimental demography of the sand-dune annual, Cakile edentula, growing along an environmental gradient in Nova Scotia. Journal of Ecology. 69:615-630.
Laing, C. 1958. Studies in the ecology of Ammophila Breviligulata. I. Seedling survival and its relation to population increase and dispersal. Botanical Gazette. June:208-216.
Lambers, H., E.S. Chapin III and T.L. Pons. 1998. Plant Physiological Ecology. Springer Publishers, New York, NY (USA).
Larcher, W. 1995. Physiological Plant Ecology (3rd edition). Springer, Berlin (DEU).
109
Loik, M.E. 2007. Sensitivity of water relations and photosynthesis to summer precipitation pulses for Artemisia tridentate and Purshia tridentate. Plant Ecology. 191:95-108.
Maun, M. 1994. Adaptations enhancing survival and establishment of seedlings on coastal dune systems. Vegetatio. 111-59-70.
Maun, M., R. Boyd, L. Olson. 1990. The biological flora of coastal dunes and wetlands. I. Cakile edentula (Bigel.) Hook. Journal of Coastal Research. 6:137-156.
McDowell, N., W. Pockman, D. Allen, D. Breshears, N. Cobb, T. Kolb, J. Plaut, J. Sperry, A.West, D. Williams. 2008. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytologist. 178: 719–739.
Moreno-Casasola, P. and G. Vazquez. 1999. The relationship between vegetation dynamics and water table in tropical dune slacks. Journal of Vegetation Science. 10:515-524.
Nobel, P.S. 1999. Physiochemical and environmental plant physiology (2nd edition). Academic Press, New York, NY (USA).
Nobel, P.S. 2002. Cacti. University of California Press, Berkeley, California (USA).
Norman, G.R.N. and D.L. Streiner. 2000. Biostatistics: the bare essentials. B.C. Decker Publishers, London (GRB).
Osmond, C.B., M.P. Austin, J.A. Berry, W.D. Billings, J.S. Boyer, J.W.H. Dacey, P.S. Nobel, S.D. Smith and W.E. Winner. 1987. Stress physiology and the distribution of plants. Bioscience. 37:38-48.
Padilla, F.M. and F.I. Pugnaire. 2007. Rooting depth and soil moisture control Mediterranean woody seedling survival during drought. Functional Ecology. 21:489-495.
Payne, A. and M. Maun. 1984. Reproduction and survivorship of Cakile edentula var. lacustris along the Lake Huron Shoreline. The American Midland Naturalist. 111(1)86-95.
Pemadasa, M. and P. Lovell. 1975. Factors affecting the distribution of some annuals in the dune system at Aberffraw, Anglesey. Journal of Ecology. 63:41-59.
Radford, A.E., H.E. Ahles and C.R. Bell. 1968. Manual of the Vascular Flora of the Carolinas. The University of North Carolina Press. Chapel Hill, North Carolina (USA).
110
Resco, V., D.D. Ignance, W. Sun, T.E. Huxman, J.F. Weltzin and D.G. Williams. 2008. Chrolorophyll fluorescence, predawn water potential and photosynthesis in precipitation pulse-driven ecosystems – implications for ecological studies. Functional Ecology. 22:479-483.
Ripley, B. and N. Pammenter. 2004. Do low standing biomass and leaf area index of subtropical coastal dunes ensure that plants have an adequate supply of water? Oecologia. 139:535-544.
Saha, S., T.M. Strazisar, E.S. Menges, P. Ellsworth and L. Sternberg. 2008. Linking the patterns in soil moisture to leaf water potential, stomatal conductance, growth and mortality of dominant shrubs in the Florida scrub ecosystem. Plant Soil. 313:113-127.
Salisbury, F.B. and C.W. Ross. 1992. Plant Physiology (4th edition). Wadsworth Publishing Company, Belmont, CA (USA).
Sanders, H.L. 1968. Benthic diversity: a comparative study. American Naturalist. 102:243-282.
Scholander, P.F., H.T. Hammel, E.D. Bradstreet and E.A. Hemingsen. 1965. Sap pressure in vascular plants. Science. 148:339-346.
Schulze, E.D., R.H. Robichaux, J.Grace, P.W. Rundel and J.R. Ehleringer. 1987. Plant water balance. Bioscience. 37:1-37.
Schwinning, S., O Sala, M. Loik and J. Ehleringer. 2004. Thresholds, memory, and seasonality: understanding pulse dynamics in arid/semi-arid ecosystems. Oecologia. 141:191-193.
Shao, G., H.H. Shugart and B.P. Hayden. 1996. Functional classification of coastal barrier island vegetation. Journal of Vegetation Science. 7:391-396.
Smith, W.K., T.C. Vogelmann, E.H. DeLucia, D.T. Bell and K.A. Shepard. 1997. Leaf form and photosynthesis. Bioscience. 47:785-793.
Smith, W.K. and N.M. Hughes. 2009. Progress in coupling plant form and photosynthetic function. Castanea. 74:1-26.
Stallman, D.A. 2004. Echoes of Topsail. Carlisle Printing, Sugarcreek, OH (USA).
Tyndall, R., A. Teramura and L. Douglas. 1986. Potential role of soil moisture deficit in the distribution of Cakile edentula. Canadian Journal of Botany. 64:2789-2791.
United States Fish and Wildlife Service. 1993. Endangered and threatened wildlife and
111 plants; Amaranthus pumilus (seabeach amaranth) determined to be threatened. Federal Register 58(65): 18035-18041.
van der Valk, A. 1974. Environmental factors controlling the distribution of forbs on coastal foredunes in Cape Hatteras National Seashore. Canadian Journal of Botany. 52: 1057-1073.
van der Valk, A. 1977. The macroclimate and microclimate of coastal foredune grasslands in Cape Hatteras National Seashore. International Journal of Biometry. 21:227-237.
Weakley, A. and M. Bucher. 1992. Status survey of seabeach amaranth (Amaranthus pumilus Rafinesque) in North and South Carolina. Report to the North Carolina Plant Conservation Program, and Endangered Species Field Office, North Carolina.
Weller, S. 1985. Establishment of Lithospermum caroliniense on sand dunes: the role of nutlet mass. Ecology. 66:6:1893-1901.
Wong, S., I. Cowan and G. Farquhar. 1979. Stomatal conductance correlates with photosynthetic capacity. Nature. 282:424-426.
Xu, H. and Y. Li. 2006. Water-use strategy of three central Asian desert shrubs and their responses to rain pulse events. Plant and Soil. 285:5-17.
Xu, H., Y. Li, G. Xu and T. Zou. 2007. Ecophysiological response and morphological adjustment of two Central Asian desert shrubs toward variation in summer precipitation. Plant, Cell and Environment. 30:399-409.
Zhang, J. 1996. Interactive effects of soil nutrients, moisture and sand burial on the development, physiology, biomass and fitness of Cakile edentula. Annals of Botany. 78:591-598.
112
Table IV-1. Average daily distribution and total monthly rainfall (cm) on Topsail Island, NC 1 July 2002 through 30 June 2003.
Measurement Period 0001-0559 0600-1159 1200-1759 1800-2400 Monthly (Solar Time) Total
July 3.54 cm 0.90 cm 2.35 cm 5.33 cm 12.12 cm
August 20.97 6.31 2.80 4.16 34.24
September 2.79 0.98 8.78 1.39 13.94
October 0.54 1.55 1.68 2.96 6.73
November 1.32 3.25 1.77 1.10 7.44
December 0.27 4.03 3.95 0.72 8.97
January 2.10 1.68 0.19 0.70 4.67
February 3.11 2.21 2.03 2.81 10.16
March 2.66 3.29 4.51 4.58 15.04
April 2.46 1.48 6.90 1.48 12.32
May 4.64 6.00 1.35 7.34 19.35
June 0.68 1.71 5.12 3.87 11.38
Yearly Total 45.08 33.39 41.45 36.44 156.36
113
Table IV-2. Soil water content (%) of 100 g substrate samples taken at different depths from Topsail Island, NC in the spring and summer of 2004. Standard errors are in parentheses.
Water Content (%) Date 10 cm 30 cm 50 cm 19 April 3.21 (0.40) 3.73 (0.24) 3.97 (0.36) 19 May 3.27 (0.40) 3.21 (0.09) 3.97 (0.79) 18 Jun 1.29 (0.40) 2.72 (0.12) 3.68 (0.45) 12 July 3.47 (0.39) 3.04 (0.18) 3.70 (0.57) Average 2.81 (0.51) 3.18 (0.21) 3.83 (0.08)
114 July 14 August 31 October 20 December 12 January 28 March 20 May 12 June 30 20 18 16 14 12 10 8 6 RAINFALL (cm) 4 2 0 0 25 50 75 100 125 150 175 200 225 250 275 300 325 350 375 DAYS
Figure IV-1. Daily rainfall totals on Topsail Island, NC from 1 July 2002 until 30 June 2003.
115
2500
2000 ) -1 s -2 12 August 2002 1500 -2 mol m mol
Total PAR = 48.76 mol m 1000 PAR ( PAR 500
0 4 8 12 16 20 SOLAR TIME (hrs X 100)
2500
2000 ) -1 s -2 26 November 2002 1500 -2 mol m mol Total PAR = 16.93 mol m 1000 PAR ( PAR 500
0 4 8 12 16 20 SOLAR TIME (hrs X 100)
2500
2000 ) -1 s 23 March 2003 -2 1500 -2 mol m mol
Total PAR = 46.90 mol m 1000 PAR ( PAR 500
0 4 8 12 16 20 SOLAR TIME (hrs X 100)
2500
2000 ) -1 s 29 June 2003 -2 1500 -2 Total PAR = 63.53 mol m m mol 1000
PAR ( PAR 500
0 4 8 12 16 20 SOLAR TIME (hrs X 100)
Figure IV-2. Photosynthetically Active Radiation (PAR) measurements taken on representative days during 2002 and 2003.
116 Overwash Period
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
senescence A. pumilus seedling flowering fruiting
C. edentula senescence
flowering/fruiting seedling seedling seedling
I. imbricata senescence
flowering fruiting seedling
H. bonariensis leaf scenescence
vegetative flowering fruiting growth
Figure IV-3. Diagramatic representation of Amaranthus pumilus, Cakile edentula, Iva imbricata, and Hydrocotyle bonariensis life-history traits on Topsail Island, NC. 117 0.0
0.2
0.4
0.6 A. pumilus 0.8 C. edentula H. bonariensis 1.0 I. imbricata
1.2
1.4 12 AUG 2002
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4 26 NOV 2002
0.0 (-MPa) 0.2
0.4
0.6
0.8
1.0
1.2
1.4 23 MAR 2003
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4 29 JUN 2003
1.6 4 8 12 16 20 SOLAR TIME (hrs X 100)
Figure IV-4. Diurnal xylem water potential (Ψ) measurements taken on representative days during 2002-2003. Bars represent standard error.
118 30
25 12 AUG 2002
20
15
10
5
0
25 26 NOV 2002
20 A. pumilus C. edentula H. bonariensis 15 I. imbricata
10 ) -1
s 5 -2 m
2 0
25 23 MAR 2003 mol CO mol 20 A (
15
10
5
0
25 29 JUN 2003
20
15
10
5
0 4 8 12 16 20
SOLAR TIME (hrs X 100)
Figure IV-5. Diurnal assimilation rates (A) taken on representative days during 2002-2003. Bars represent standard error.
119 200
A. pumilus 175 12 AUG 2002 C. edentula H. bonariensis 150 I. imbricata
125
100
75
50
25
0
175 26 NOV 2002
150
125
100
75
50 ) -1 s 25 -2 -2
0
175 23 MAR 2003 g (mmol m g (mmol
150
125
100
75
50
25
0
175 29 JUN 2003
150
125
100
75
50
25
0 4 8 12 16 20 SOLAR TIME (hrs X 100)
Figure IV-6. Diurnal stomatal conductance rates (g) taken on representative days during 2002-2003. Bars represent standard error.
120 4.0
3.5 12 AUG 2002
3.0
2.5
2.0
1.5
1.0
0.5
0.0
3.5 26 NOV 2002 A. pumilus 3.0 C. edentula H. bonariensis 2.5 I. imbricata
2.0
1.5
1.0 ) -1 0.5 s -2
0.0
3.5 23 MAR 2003 E (mmol m E (mmol
3.0
2.5
2.0
1.5
1.0
0.5
0.0
3.5 29 JUN 2003
3.0
2.5
2.0
1.5
1.0
0.5
0.0 4 8 12 16 20 SOLAR TIME (hrs X 100)
Figure IV-7. Diurnal transpiration rates (E) taken on representative days during 2002-2003. Bars represent standard error.
121 rain event
0.0
0.2
0.4
0.6
0.8 (-MPa) 1.0
1.2
1.4
1.6
25 A. pumilus C. edentula H. bonariensis )
-1 20 I. imbricata s -2 m 2 15 mol CO mol 10 A (
5
0
175
150 )
-1 125 s -2
100
75 g (mmolm
50
25
0
3.5
3.0 )
-1 2.5 s -2 2.0
1.5 E (mmol m
1.0
0.5
0.0 4 8 12 16 20 SOLAR TIME (hrs X 100)
Figure IV-8. Diurnal xylem water potential measurements (Ψ), assimilation rates (A), conductance rates (g) and transpiration rates (E) taken on 21 Jun 2002. A rain event totaling 0.80 cm occurred from 1430 to 1500 Solar Time.
122 CHAPTER V
USE OF PHOTOSYNTHETIC CARBON GAIN AS A COMMON CURRENCY:
MODELING RESPONSE OF FOUR PLANT SPECIES TO THE PRESENT DAY
BARRIER ISLAND BEACH ENVIRONMENT
Introduction
For many years researchers have been interested in identifying parameters that are important indicators of plant success in various environments (Salisbury and Ross 1992,
Larcher 1995, Lambers et al. 1998, Barbour et al. 1999). Specific leaf area (Korner
1991), internal leaf anatomy and development (Oguch et al. 2008), carbon allocation patterns (Smith and Stitt 2007) biomass (Barbour et al. 1985), respiration rate (Nobel
1995), biochemistry (Evans et al. 1995), water relations (Schulze et al. 1987) and photosynthetic carbon gain (PCG) (Crawford 2008) are a few of the parameters that have been used. Taken alone, none of these can provide a complete picture of plant success in a given environment.
For more than two decades, researchers have been calling for studies that incorporate multiple variables and assess several factors when defining plant success
(Chapin III et al. 1987, Osmond et al. 1987, Korner 1991, Ackerly et al. 2000). Such studies are ideal, but are necessarily large in scope often requiring significant resources that may call the cost to benefit ratio into question. Of all the single factors linked to plant success, PCG has enjoyed the most widespread usage (Lee and Ignaciuk 1985,
Pearcy et al. 1987, Crawford 2008). As with any single parameter, there are limitations
123 to the applicability of PCG and results must therefore be interpreted carefully (Osmond et al. 1987, Korner 1991, Oguchi et al. 2008).
Photosynthetic carbon gain has been linked to plant fitness in a number of studies
(Pearcy et al. 1987 and references therein, Oguchi et al. 2008, Nilsen et al 2009, Russell
et al. 2009), although it is necessary for researchers to clearly define what is meant by
“fitness” (Barbour et al. 1999 and references therein, Arntz et al. 2000). Some authors
have questioned the existence of a direct relationship between PCG and fitness stating the
need to include various other variables depending upon the specific study – or specialty of the researcher (Larcher et al. 1995 and references therein, Arntz et al. 1998, Gassmann
2004). Despite all of these concerns, PCG has been shown to be a relatively efficient and effective proxy for the estimation of plant success/fitness in several environments
(Solbrig 1981, Lechowicz and Blais 1988, Gerber 1990, Cheplick 1995, Lambers et al.
1998 and references therein).
Barrier island (BI) beach ecosystems have traditionally been viewed as harsh, transient and physically controlled habitats where only a small suite of plant species
survive (Sanders 1968, Barbour et al. 1985, Lee and Ignaciuk 1985, Weakley and Bucher
1992, Hancock and Hosier 2003). Although general ecological and life-history models
for some BI beach plant species have been proposed (Dubois 1977, Ehrenfeld 1990 and
references therein, Maun et al. 1990 and references therein, Evans and McCain 1995),
none have incorporated ecophysiological concepts such as PCG. Such models would
provide a general understanding of how plants respond to the current daily, seasonal and
episodic stresses of the BI beach environment. Baselines established from these studies
could be used to predict BI beach plant response to future climate change – an especially
124 important topic due to the sensitivity of this habitat to sea level rise and extreme episodic
storm events (Schoenbaum 1982, Feagin et al. 2009).
Quantifying limitations to PCG where possible and qualitatively describing them elsewhere (Pilkey and Pilkely-Javis 2008) would strengthen the models, making them
more robust. Several barrier beach studies, both on the West Coast of the USA (DeJong
1978a, DeJong 1978b, Mooney et al. 1983) and Japan (Ishikawa et al. 1990, Ishikawa et al. 1991, Ishikawa et al. 1996), have related reductions in photosynthesis to various environmental stresses. These studies did not directly address limitations to PCG nor place findings in a larger context (e.g. ecophysiological models), although researchers in other environments have done so (Johnson et al. 2004, Quero et al. 2008).
The purposes of the present study were to:
1. Quantify PCG of four BI beach species representing distinct functional plant groups
(as defined by Shao et al. 1996, Crawford 2008)
2. Quantitatively and/or qualitatively describe limitations to PCG
3. Develop conceptual models incorporating abiotic stressors, plant response and species fitness in the BI beach environment
Materials and Methods
Study Site
Topsail Island is a low topographic relief, 42 km long BI that varies in width from
150 to 500 m located approximately 40 km northeast of Wilmington, North Carolina
(Stallman 2004). The island is extensively developed with single family homes along almost its entire length (Frankenburg 1997). The study site was located on the southwestern end of the island (34o 20’ 50” N, 77o 39’ 5” W) adjacent to New Topsail
125 Inlet. Due to migration of the inlet to the southwest at an average rate of 35 m per year,
an extensive beach and dune environment extends approximately 1-2 km from the inlet to
the first beach home.
Species
Amaranthus pumilus (Rafinesque) is a pioneering C4 annual species that inhabits
the driftline and foredune area of the BI beach (Weakley and Bucher 1992). The plant
has a prostrate growth form, succulent leaves and pink to reddish stems. As a result of
population decline due to habitat loss, A. pumilus was listed as federally threatened in
1993 (Weakley and Bucher 1992, United States Fish and Wildlife Service 1993). Cakile
edentula (Bigelow) Hooker is a pioneering C3 annual species that has an upright growth
form and succulent leaves (Radford et al. 1968). The plant is common within its range
(Barbour and Rodman 1970) and unlike A. pumilus, C. edentula can persist into a second
growing season in moderate climates (Barbour and Rodman 1970, Boyd and Barbour
1993, Cody and Cody 2004). Hydrocotyle bonariensis Lamarck is a C3 perennial species
whose seeds germinate in swales located landward of the primary dune on BI beaches
(Evans 1992). Plants often grow seaward into the foredune via rhizomes (Evans 1992).
Leaves are peltate, vary in width from 4 to 12 cm and senesce in winter with the rhizomes persisting underground until the next growing season (Radford et al. 1968). Iva imbricata Walter is a succulent leaved, woody C3 shrub that can grow to heights of 1 m
and widths of 3 m (Radford et al. 1968). As a seedling, I. imbricata coinhabits the
driftline with A. pumilus and C. edentula.
The Sunlight Environment
126 Continuous measurements of Photosynthetically Active Radiation (PAR) were
taken from June 2002 until June 2004 using a LI-190 Quantum Sensor (Li-Cor, Lincoln
Nebraska) mounted on a 1.5 m wooden pole (10 cm X 10 cm) interfaced with a HOBO data logger via a Universal Transconductance Amplifier (EME Systems, Berkley CA).
Photosynthetic Carbon Gain (PCG)
Gas exchange measurements were taken approximately every three hours from dawn until dusk on one representative day each month from 21 June 2002 until 20 May
2003. The first fully expanded leaf of five different individuals for each species was measured using the TPS Portable Photosynthesis System (PP Systems, Amesbury,
Massachusetts). Photosynthesis (A) was calculated from the CO2 flux rate. Total daily
-2 -1 assimilation (mol CO2 m day ) was quantified by determining the area under the
diurnal photosynthesis curve (assimilation X solar time) for each measurement day.
-2 -1 Total monthly assimilation (mol CO2 m month ) was calculated by multiplying total
daily assimilation times the number of days in that particular month.
Photosynthetic Light Response
Photosynthetic light response of the adaxial leaf surface of each species was measured using the Transportable Photosynthesis System. The first fully expanded leaf
of approximately thirty individuals of each species was chosen for measurement. Neutral density filters were used to attenuate natural light resulting in PAR values ranging from
2000 μmol m-2 s-1 (full sun) to 100 μmol m-2 s-1. Leaves were allowed to acclimate to new light intensities for two minutes between readings. Previous measurements have shown that leaves return to a maximum photosynthetic rate for a given PAR value within two minutes and that order of light attenuation (high to low, low to high, or random) does
127 not affect readings. Measurements were taken on 7 July 2002 between 1000 and 1200 hours (solar time). Best-fit linear and quadratic regression equations were used to describe the relationship between PAR and photosynthesis (i.e. assimilation rate, A).
Due to the quadratic relationship between A and PAR for H. bonariensis, assimilation rates were log10 transformed (Norman and Streiner 2000). The relationship between A and PAR for all other species was linear. The A:PAR ratio for each species was then determined and tested for significant differences using a single-factor ANOVA
(MacDonald 2008).
Predicted versus Actual PCG
Daily PCG was predicted for each species on 29 June 2003 by entering PAR values (see The Sunlight Environment) into the best-fit linear and quadratic photosynthetic light response regression equations (see Photosynthetic Light Response).
This generated a daily photosynthesis curve whose area represented predicted PCG (see
Quero et al. 2008 for a similar experimental set-up). Actual PCG was determined via the methods described in the Photosynthetic Carbon Gain section.
Transplantation Experiment
One-hundred and fifty A. pumilus seedlings (approximately twenty leaf-stage) were obtained from the New Hanover/Brunswick County Cooperative Extension greenhouse located on Oak Island, NC. Seedlings were grown from seeds collected on
Oak Island (approximately 60 miles southwest of Topsail Island). Past studies have indicated that differences between populations of A. pumilus living on Oak Island and
Topsail Island should be minimal (Weakley and Bucher 1992, Strand 2002). On 18 June
2004, forty-four plants were transplanted to each of three experimental sites (site 1 =
128 driftline, site 2 = foredune, site 3 = primary dune) on the southwestern end of Topsail
Island. Eighteen of the original one-hundred and fifty plants were not used due to signs of stress/decline (yellowing leaves, stunted growth). Forty-four naturally occurring A. pumilus plants were also observed and measured. Each plant received supplemental water (to field capacity) – once at transplantation and once later the same day at
approximately 1800 solar time. Observations of the plants, including number surviving
and general appearance, were made on 14 July, 11 August and 4 September 2004. Gas
exchange measurements were taken on 14 July 2004 using the same protocol as depicted in the Photosynthetic Carbon Gain section.
Results
The Sunlight Environment
Figure V-1 shows PAR measurements taken on four representative days during
-2 2002-2003. Actual PAR (PARA) measured on 12 August 2002 was 48.76 mol m , while theoretical PAR (PART), maximum amount of PAR given a completely clear sky throughout the day, was 57.37 mol m-2. Passing clouds accounted for the difference
between PARA and PART (a 15% reduction in total radiation for the day). PARA for 26
-2 -2 November 2002 was 16.93 mol m while PART was 28.40 mol m (a 40% reduction due
-2 -2 to clouds). PARA for 23 March 2003 was 46.90 mol m while PART was 51.55 mol m
(a 9% reduction due to clouds). In the final representative day, PARA for 29 June 2003
-2 -2 was 63.53 mol m while PART was 64.50 mol m (a 1.5% reduction due to clouds).
Photosynthetic Carbon Gain (PCG)
Figures V-2a, V-2b and V-2c depict diurnal assimilation measurements (diurnal
photosynthesis curves) for A. pumilus, C. edentula, H. bonariensis and I. imbricata taken
129 on one representative day per month from 21 June 2002 until 20 May 2003. Amaranthus
-2 -1 pumilus had the highest assimilation rate (17 μmol CO2 m s ) of any species on 21 June
-2 -1 2002. Iva imbricata had the second highest rate (14 μmol CO2 m s ) with C. edentula
-2 -1 and H. bonariensis assimilation rates being essentially equal (7 μmol CO2 m s ). On 3
July 2002, maximum assimilation rates for A. pumilus, C. edentula and I. imbricata were
-2 -1 15-16 μmol CO2 m s , with I. imbricata rates declining quickly in the afternoon hours.
-2 -1 The maximum rates of H. bonariensis were substantially lower (7 μmol CO2 m s ) than the other three species. Amaranthus pumilus again had the highest assimilation rates on
-2 -1 12 August 2002 (19 μmol CO2 m s ), followed by I. imbricata and H. bonariensis
-2 -1 (approximately 9 μmol CO2 m s ). Cakile edentula was absent during this time period.
During 17 September 2002, the maximum assimilation rate of I. imbricata was 15 μmol
-2 -1 -2 -1 CO2 m s followed by H. bonariensis (9 μmol CO2 m s ) and A. pumilus (5 μmol CO2
m-2 s-1). Cakile edentula was again absent during this time period.
On 21 October, 26 November and 17 December 2002, C. edentula, H. bonariensis
and I. imbricata were present, but had low assimilation rates throughout the day (3 μmol
-2 -1 -2 -1 -2 -1 CO2 m s , 5 μmol CO2 m s and 5 μmol CO2 m s maximum, respectively).
Amaranthus pumilus was absent during both measurement periods. Only C. edentula was present on 15 January 2002, 4 February and 23 March 2003 when maximum assimilation
-2 -1 -2 -1 -2 -1 rates of 5 μmol CO2 m s , 4 μmol CO2 m s and 11 μmol CO2 m s were recorded,
respectively.
Cakile edentula, H. bonariensis and I. imbricata had very similar diurnal
assimilation rates throughout the day on 17 April 2003, reaching a maximum of
-2 -1 approximately 5 μmol CO2 m s at 1200 solar time. Amaranthus pumilus was not
130 present during this measurement period. On 20 May 2003, A. pumilus experienced the
-2 -1 highest assimilation rate (25 μmol CO2 m s ) of any species. The maximum rates of C.
-2 -1 edentula and I. imbricata were equivalent (17-18 μmol CO2 m s ) while H. bonariensis
-2 -1 had lower maximum values (13 μmol CO2 m s ).
Total daily assimilation (area under each of the diurnal photosynthesis curves
mentioned above) for A. pumilus, C. edentula, H. bonariensis and I. imbricata is shown
in Table V-1. Amaranthus pumilus was present during five of the measurement periods,
-2 assimilating the greatest amount of CO2 (0.74 mol m ) on 20 May 2003 and the least
(0.12 mol m-2) on 17 September 2002. Cakile edentula was present during ten of the
-2 measurement periods, assimilating the greatest amount of CO2 (0.54 mol m ) on 20 May
2003 and the least (0.09 mol m-2) on 21 October 2002. Hydrocotyle bonariensis was present during ten of the measurement periods, assimilating the greatest amount of CO2
(0.45 mol m-2) on 20 May 2003 and the least (0.07 mol m-2) on 21 October 2002. Iva
imbricata was present during nine of the measurement periods, assimilating the greatest
-2 -2 amount of CO2 (0.62 mol m ) on 20 May 2003 and the least (0.09 mol m ) on 21
October 2002.
Total monthly assimilation, computed by multiplying the total daily assimilation
times the number of days in a particular month, for A. pumilus, C. edentula, H.
bonariensis and I. imbricata is show in Table V-2. Obviously the yearly patterns of high
and low monthly assimilation mirror those of daily assimilation for each species. Using
this calculation method, I. imbricata had the highest total yearly assimilation (80.16 mol
-2 -1 -2 -1 CO2 m s ), C. edentula had the second highest (69.91 mol CO2 m s ) with A. pumilus
131 -2 -1 having the third highest (63.14 mol CO2 m s ) and H. bonariensis the least (59.10 mol
-2 -1 CO2 m s ).
Photosynthetic Light Response
The photosynthetic light response of each species is illustrated in Figure V-3.
The slope of the best-fit line for A. pumilus and I. imbricata photosynthetic light response were the steepest of any species measured and not significantly different from one another, (F = 2.16, p = 0.15), with no evidence of light saturation. Maximum
-2 -1 assimilation rates of A. pumilus were approximately 24 μmol CO2 m s obtained at
PAR values of 1800 μmol m-2 s-1. Maximum assimilation rates for I. imbricata were 22
-2 -1 -2 -1 μmol CO2 m s obtained at a PAR value of 1600 μmol m s . The slope of the best fit
line for C. edentula was less steep than the best-fit line for A. pumilus (F = 48.88, p <
0.001) and I. imbricata (F = 19.46, p < 0.001), with no evidence of light saturation.
-2 -1 Maximum assimilation rates of C. edentula were approximately 12 μmol CO2 m s obtained at PAR values of 1600 μmol m-2 s-1. The relationship between assimilation and
PAR for H. bonariensis was quadratic and therefore did exhibit light saturation at PAR
values greater than 900 μmol m-2 s-1. Maximum assimilation rates for H. bonariensis
-2 -1 were approximately 9 μmol CO2 m s . Equations for the best fit line or curve can be
found in Table V-3.
Predicted versus Actual PCG
Figure V-4 shows predicted and actual PCG for A. pumilus, C. edentula, H.
bonariensis and I. imbricata. Based upon the photosynthetic light response of A. pumilus
-2 -1 and PAR values for 29 June 2003, predicted PCG was 1.00 mol CO2 m s while actual
-2 -1 measurements for the same day were 0.44 mol CO2 m s (a negative difference of
132 -2 -1 66%). In the same manner, the predicted PCG for C. edentula was 0.46 mol CO2 m s
-2 -1 while the actual PCG was 0.52 mol CO2 m s (a positive difference of 21%). The
-2 -1 predicted PCG for H. bonariensis was 0.36 mol CO2 m s while the actual PCG was
-2 -1 0.19 mol CO2 m s (a negative difference of 47%). Finally, the predicted PCG for I.
-2 -1 -2 -1 imbricata was 1.00 mol CO2 m s while the actual PCG was 0.40 mol CO2 m s (a negative difference of 60%).
Transplantation Experiment
Figure V-5 is a schematic diagram of the three transplantation sites as well as a table depicting the number of plants surviving during each observation period. Of the forty-four naturally occurring A. pumilus plants followed through the season, thiry-four were present on 14 July, twenty-nine on 11 August and thirteen on 4 September 2004. Of the forty-four plants transplanted to site 1 (driftline), thirty-three were present on 14 July, twenty-six on 11 August and ten on 4 September 2004. Of the forty-four plants transplanted to site 2 (foredune), forty-three were present on 14 July, forty-two on 11
August and zero on 4 September 2004. Of the forty-four plants transplanted to site 3
(primary dune), forty-two were present on 14 July, forty-one on 11 August and zero on 4
September 2004.
Figure V-6 depicts diurnal photosynthesis for representative A. pumilus plants at each of the transplantation sites as well as individuals found naturally growing in the driftline and foredune habitats taken on 14 July 2004. The naturally occurring plants
-2 -1 reached a maximum photosynthetic rate of 22 µmol CO2 m s by 1200 solar time. The
diurnal photosynthetic rates of the driftline and foredune transplants were comparable,
-2 -1 reaching a maximum of approximately 14 µmol CO2 m s at 1200 solar time, although
133 the photosynthetic rate of the foredune transplants did decrease more rapidly than the
driftline transplants in the afternoon/evening. The diurnal photosynthetic rate of the
- primary dune transplants was substantially lower, reaching a maximum of 6 µmol CO2 m
2 -1 s by 1200 solar time. Photosynthetic carbon gain on 14 July 2004 was 0.479 mol CO2
-2 -1 -2 -1 -2 -1 -2 -1 m day , 0.337 mol CO2 m s , 0.146 mol CO2 m s and 0.579 mol CO2 m s for
driftline, foredune, primary dune and natural A. pumilus plants, respectively.
Discussion
Photosynthetic Carbon Gain (PCG)
The daily patterns of PCG for each species were influenced by both physiology
and life-history traits (Figures V-2a, b and c; Table V-1; for a full discussion of
physiology and life-history of each species see Chapter IV). For example, A. pumilus had the highest assimilation rates in the months of May, June, July and August but by
September rates had noticeably declined. By October all A. pumilus plants were gone from the study site. Cakile edentula exhibited moderate to high assimilation rates and was absent during some of the hottest months of the year, late July, August and
September, when the vapor pressure deficit and hence transpiration would have been very high. Iva imbricata also had moderate to high assimilation rates and was absent during
January, February and March. Finally, assimilation measurements for H. bonariensis were the lowest recorded. Hydrocotyle bonariensis was present during all months except
January and February.
Table V-2 depicts the estimated yearly PCG for each plant. Although these estimations are based on only one actual measurement day per month and these measurement days were necessarily sunny to partly cloudy (due to the inability of taking
134 gas exchange measurements during a rainy day), they still offer a good starting point to
discuss yearly PCG. Perhaps each of these BI beach species must reach a yearly PCG
threshold that is species specific in order to complete their life cycle (or survive into a
second year if they are perennials), as has been demonstrated in other plants (Pearcy et al.
-2 -1 1987, Larcher 1995). The yearly PCG of A. pumilus was 63.14 mol CO2 m yr while
-2 -1 that of C. edentula, H. bonariensis and I. imbricata were 69.91 mol CO2 m yr , 59.10
-2 -1 -2 -1 mol CO2 m yr and 80.16 mol CO2 m yr , respectively. What is interesting is how
each species obtained these totals. Amaranthus pumilus assimilated all of its carbon via
high photosynthetic rates within a five to six month time period. Cakile edentula had
lower overall photosynthetic rates but was active during nine to ten months of the year.
Iva imbricata exhibited relatively high photosynthetic rates and was active during nine
months of the year. The photosynthetic rates of Hydrocotyle bonariensis were low, but
the plant remained active during ten months of the year.
The yearly PCG threshold for A. pumilus and C. edentula are comparable possibly
because both plants have similar life-styles and associated structural/allocation costs
(both plants are annuals and are similar in size and weight at maturity). The yearly PCG
threshold for H. bonariensis is slightly less than the other three species possibly because
of reduced above ground structure and therefore lower associated costs. Finally, the
yearly PCG threshold for I. imbricata is the highest potentially due to the high associated
costs of producing and maintaining substantial perennial above-ground biomass. Several
studies have linked increased PCG thresholds to increased structural costs (Lambers et al.
1998, Barbour et al. 1999, Crawford 2008). Differences in structure (annual, perennial,
135 herbaceous, woody, growth form) are often used to organize species into functional plant
groups (Shao et al. 1996, Crawford 2008).
Perhaps there exists PCG thresholds that relate to plant life-history stages. For
example, maybe A. pumilus seedlings must assimilate a given amount of carbon before
they can move to the pre-reproductive stage which includes stem and root elongation as
well as leaf development (Weakley and Bucher 1992, Hancock and Hosier 2003).
Another potential stage might ocurr when flowers and fruits are produced. After plants
become reproductive then maintenance until senescence could be been an important concept to consider in relation to carbon requirements. Figure V-7 provides a conceptual model for how PCG thresholds and maintenance demands potentially relate to life-history
stages in A. pumilus. A variety of studies have examined life-history stages in plants and
found correlations between PCG and leaf age (Zhang et al. 2008, Reich et al. 2009),
water status (Casper et al. 2006, Reinhardt et al. 2009) and reproduction (Arntz et al.
1998). Of course, PCG is only one part of a much larger, complete story that includes
allocation patterns and metabolic costs (Korner 1991, Larcher 1995).
Limitations to PCG
The photosynthetic light response of each species taken on 7 July 2002 (Figure V-
3) coupled with PAR measurements taken on 29 June 2003 (Figure V-1) were used to
generate predicted PCG for a typical day on Topsail Island, NC (Figure V-4). Predicted
PCG values deviated widely from actual values, over-estimating for three species and
under-estimating for one. These results lead to the obvious conclusion that many
environmental factors besides irradiance levels influence photosynthesis rates and hence
PCG in these four BI beach species. Cakile edentula was the lone species in which actual
136 PCG was higher than potential PCG and this may be attributed to differences in life history patterns. Cakile edentula is dormant (survives only as a seed) during late July into late October whereas the other three species are active during this time period. The photosynthetic light response measurements used to calculate the predicted PCG were taken on 7 July 2002 possibly when C. edentula plants were beginning to senesce. This would cause the assimilation values in relation to PAR values to be lower than if measurements were taken earlier in the year, substantially reducing predicted PCG.
Amaranthus pumilus, H. bonariensis and I. imbricata plants were actively growing during this time period therefore photosynthetic light response values were relatively high resulting in higher predicted PCG.
Between 17 June and 11 August 2004, natural A. pumilus plants and driftline transplants experienced similar die-offs of 34% and 41%, respectively (Figure V-5).
During the same time period, foredune and primary dune transplants experienced 5% and
7% die-offs, respectively. By the final survey on 9 September 2004, however, 30% of the natural A. pumilus plants and 23% of the driftline transplants were present while none of the foredune or primary dune transplants were present. A potential explanation for this difference is illustrated in Figure V-6. On 14 July 2004, naturally occurring A. pumilus plants had the highest PCG followed by driftline, foredune and primary dune transplants.
This pattern mirrors the abundance of naturally occurring A. pumilus plants on at least eight BI beaches located in southeastern NC, with the vast majority of plants found along the driftline, some found in the foredune and a rare few found in the primary dune
(personal observation). Assuming that seed dispersal to these three habitats is relatively equal as has been suggested by several authors (Ehrenfeld 1990, Maun et al. 1990,
137 Weakley and Bucher 1992, Hancock and Hosier 2003), microscale differences in abiotic factors may account for differential PCG and survival. Several reviews have reached similar conclusions based on studies from a variety of environments (Pearcy et al. 1987,
Baskin and Baskin 1998, Clark et al. 2007).
Factors that have been shown to limit growth of beach plants in specific situations include drought (Ishikawa et al. 1996), salinity (De Jong 1978, Ishikawa et al. 1991), salt- spray (Oosting 1945, Boyce 1954, Barbour 1978), low nutrients (Barbour et al. 1985,
Barbour et al. 1999) high temperatures (Mooney et al. 1983) and salt-water overwash
(Hesp 1991, Lee and Ignaciuk 1985, Hancock and Hosier 2003). Interestingly, an
increase in the growth rate of some beach species has been associated with sand burial
(Yuan et al. 1993, Perumal and Maun 2006, Gilbert et al. 2008, Gilbert and Ripley 2008).
Although growth rate reductions have been addressed, no studies have quantified
PCG loss in relation to these abiotic factors. Indeed, the current study has in no way
quantitatively assessed reduction in PCG of A. pumilus due to any of the above factors.
However, this research has found that irradiance levels alone do not accurately predict
PCG (indicating other factors are important) and that PCG (and survival) of transplants
follows naturally occurring abundance patterns (driftline>foredune>primary dune). It
would be advisable to pursue future research that first independently tests the effect of
each factor on PCG of a selected species (e.g. A. pumilus) then tests the effects of multiple factors on PCG of the selected species (as recommended by Chapin et al. 1987 and Osmond et al. 1987).
In an excellent example of a one-factor test, Snow (unpublished data) measured the photosynthetic light response of both saltwater inundated and non-inundated A.
138 pumilus plants following a 9 July 2004 overwash event on Topsail Island, NC (Figure V-
8). Assimilation rates of saltwater inundated plants were as much as 56% lower than
non-inundated plants. Although not directly assessed, these limits to assimilation
probably reduce daily PCG potentially to the point of plant death. In a 2003 study,
Hancock and Hosier discovered that one of the major causes of A. pumilus mortality on
Figure Eight Island, NC was overwash by late summer/early fall storms. The authors
concluded that overwash (along with other abiotic factors) could theoretically cause up to
a 98% reduction in reproductive output depending upon the timing of storms. Increases
in storm intensity coupled with sea-level rise due to global climate change (IPCC 2007) is
cause for concern over the future of BI beach species, especially A. pumilus which is
currently listed as Federally Threatened (US Fish and Wildlife Service 1993).
As evidenced by the examples above, past BI studies have been able to address
the effect of certain abiotic factors on assimilation, plant mortality and reproduction.
What is lacking, along with data concerning multiple-factor effects on BI beach plants, is
a comprehensive framework in which to integrate the ideas of potential PCG, realized
PCG and species fitness. The following section introduces conceptual models intended
to serve as starting points for addressing these issues.
Modeling Abiotic Stressors, Plant Response and Species Fitness in the BI Beach
Environment
Amarathus pumilus, C. edentula, H. bonariensis and I. imbricata can be
considered representatives of four distinct functional plant groups that experience harsh daily, seasonal and extreme event stresses within the highly dynamic BI beach environment. These species exhibit a variety of stress responses that include specific leaf
139 anatomy and orientation properties (Chapter III), physiologies (Chapter IV) and life-
history patterns (Chapter IV). It can be argued that plant response to an environment
should maximize PCG, or minimize loss depending upon point of view, if there are
appreciable links to plant fitness/success. Indeed, there has been a recent emphasis in
plant research to identify important plant ecophysiological traits, define their relationship to PCG and determine their impact on plant fitness (Arntz and Delph 2001, Gerber and
Griffen 2003, Reich et al. 2003, Shipley et al. 2005, Donovan et al. 2009). The ultimate
goal of such studies is to directly link functional traits to fitness and thereby begin to
address the evolution of such traits (Ackeryl et al. 2000, Ackerly and Monson 2003).
Figure V-9 is a conceptual model of BI beach environmental stresses, species
response and resultant PCG. The general idea of the model is that BI beach plants have a
potential PCG they could attain (measured on a daily, monthly and/or yearly timeframe) if all abiotic factors were at an optimum for the particular plant species. Abiotic
environmental stresses (the environmental stress “filter” or “filters”) challenge plants
resulting in limited resource acquisition and increased resource expenditure. Plant
response (leaf anatomy/orientation, physiology and life-history patterns) to these challenges determines realized PCG. Each response is controlled by genes and therefore a plant’s individual genetic compliment in part determines response effectiveness
(Colmer and Voesenek 2009, Papdi et al. 2009, Xiao et al. 2009). At the population level selection for the “best” response (ecophysiological trait) can occur (Ackerly et al. 2000,
Arntz et al. 2000, Arntz and Delph 2001, Reich et al. 2003). Figure V-10 is intended to serve as a summary diagram relating abiotic stresses, plant response, PCG, allocation patterns and fitness in the BI beach environment
140 Although serving as a good beginning, there are several points that need to be
resolved concerning these conceptual models. Research that directly ties PCG to species
fitness is needed. Indeed, a clear definition of species fitness in the BI beach
environment should be developed. Studies in other environments have used seed number
(Gerber and Griffin 2003), vegetative biomass (Ackerly et al. 2000), life-time leaf net
carbon fixation (Shipley et al. 2005) and even photosynthetic rate (Artnz et al. 2000) as
proxies for fitness. Path analysis has been employed in several studies and offers a detailed description of individual factors and their contribution to overall fitness (Norman and Streiner 2000, Arntz and Delph 2001).
In conclusion, PCG is potentially the most efficient single parameter in which to assess plant fitness/success in the BI beach environment. This study has provided baseline PCG estimations of four plants that represent distinct functional groups located on Topsail Island, NC, explored abiotic stress (daily, seasonal and episodic) limitations to
PCG, plant response to these stresses and overall impacts on plant fitness. Conceptual
models have been presented that relate abiotic stress, plant response and fitness in the BI
beach environment. Although the information presented in this study is preliminary in
many respects and issues/questions remain, as well as the need for more detailed
research, the main ideas serve as a beginning to address the role and eventually the
evolution of functional traits in BI beach plants.
Literature Cited
Ackerly, D.D., S.A. Dudley, S.E. Sultan, J. Schmitt, J.S. Coleman, C.R. Linder, D.R. Sanquist, M.A. Gerber, A.S. Evans, T.E. Dawson and M.J. Lechowicz. 2000. The evolution of plant ecophysiological traits: recent advances and future directions. Bioscience. 50:979-995.
Ackerly, D.D. and R.K. Monson. 2003. Waking the sleeping giant: the evolutionary
141 foundations of plant function. International Journal of Plant Science. 164:S1-S6.
Arntz, A.M. and L.F. Delph. 2001. Pattern and process: evidence for the evolution of photosynthetic traits in natural populations. Oecologia. 127:455-467.
Arntz, A.M., E.H. DeLucia, N. Jordan. 1998. Contribution of photosynthetic rate to growth and reproduction in Amaranthus hybridus. Oecologia. 127:455-467.
Arntz, A.M, E.H. DeLucia, N. Jordan. 2000. From fluorescence to fitness: variation in photosynthetic rate affects fecundity and survivorship. Ecology. 81:2567-2576.
Barbour, M., J. Burk, W. Pitts, F. Gilliam and M. Schwartz. 1999. Terrestrial plant ecology (3rd edition). Benjamin Cummings Publishers, Menlo Park, CA (USA).
Barbour, M.G., T.M. DeJong and B.M. Pavlik. 1985. Marine beach and dune plant communities in B.F. Chabot and H.A. Mooney [editors], Physiological Ecology of North American Plant Communities. Pages 296-322. Chapman and Hall, New York, New York (USA).
Barbour, M. and J. Rodman. 1970. Saga of the west coast sea-rockets: Cakile edentula ssp. californica and C. maritima. Rhodora 72:370-386.
Baskin, C.C. and J.M. Baskin. 1998. Seeds: Ecology, Biogeography and Evolution of Dormancy and Germination. Academic Press, New York, NY (USA).
Boyd, R.S. and M.G. Barbour. 1993. Replacement of Cakile edentula by C. maritima in the strand habitat of California. The American Midland Naturalist. 130:209-228.
Boyce, S.G. 1954. The salt spray community. Ecological Monographs. 24:29-67.
Casper, B.B., I.N. Forseth and D.A. Wait. 2006. A stage-based study of drought response in Cryptantha flava (Boraginaceae): gas exchange, water use efficiency and whole plant performance. 93:977-987.
Chapin III, F.S., A.J. Bloom, C.B. Field and R.H. Waring. 1987. Plant responses to multiple environmental factors. Bioscience. 37:49-57.
Cheplick, G.P. 1995. Life history trade-offs in Amphibromus scabrivalvis (Poaceace): allocation to clonal growth, storage and cleistogamous reproduction. American Journal of Botany. 82:621-629.
Clark, C.J., J.R. Poulsen, D.J. Levey and C.W. Osenberg. 2007. Are plant populations seed limited? A critique and meta-analysis of seed addition experiments. The American Naturalist. 170:128-142.
Cody, M.L. and T.W.D. Cody. 2004. Morphology and spatial distribution of alien
142 searockets (Cakile spp.) on South Australian and Western Canadian beaches. Australian Journal of Botany. 52:175-183.
Colmer, T.D. and L.A.C.J. Voesenek. 2009. Flooding tolerance: suites of plant traits in variable environments. Functional Plant Biology. 36:665-681.
Crawford, R.M.M. 2008. Plants at the Margin. Cambridge University Press, Cambridge (GBR).
DeJong, T.M. 1978a. Comparative gas exchange of four California beach taxa. Oecologia. 34:343-351.
DeJong, T.M. 1978b. Comparative gas exchange and growth responses of C3 and C4 beach species grown at different salinities. Oecologia. 35:59-68.
Donovan, L.A., F. Ludwig, D.M. Rosenthal, L.H. Rieseberg and S.A. Dudley. 2009. Phenotypic selection on leaf ecophysiological traits in Helianthus. New Phytologist. 183:868-879.
Dubois, S.J. 1977. Comparative ecophysiology of C3 and C4 sand dune plant species of the Georgia coast. Master’s Thesis. University of Georgia, Athens, Georgia (USA).
Ehrenfeld, J.G. 1990. Dynamics and processes of barrier island vegetation. Aquatic Sciences. 2:437-480.
Evans, J.P. 1992. The effect of local resource availability and clonal integration on ramet morphology in Hydrocotyle bonariensis. Oecologia. 89:265-276.
Evans, J.P. and M.L. Cain. 1995. A spatially explicit test of foraging behavior in a clonal plant. Ecology. 76:1147-1155.
Evans, J.R., I. Jakobsen and E. Orgen. 1995. Carbon fixation profiles do reflect light absorption profiles in leaves. Australian journal of plant physiology. 22:865-873.
Feagin, R.A., W.K. Smith, N.P. Psuty, D.R. Young, J.C. Gibeaut, M.L. Martinez, K.F. Nordstrom, N.L, Jackson, G.A. Carter. J.N. Gemma, R.E. Koske, D.H. Thomas, J.C. Whitehead and K.L. Lucas. 2009. Journal of coastal research (in press).
Frankenburg, D. 1997. The Nature of North Carolina’s Southern Coast. The University of North Carolina Press, Chapel Hill, North Carolina (USA).
Gassmann, A.J. 2004. Effect of photosynthetic efficiency and water availability on tolerance of leaf removal in Amaranthus hybridus. Journal of Ecology. 92:882- 892.
143 Gerber, M.A. 1990. The cost of meristem limitation in Polygonum arenastrum: negative genetic correlations between fecundity and growth. Evolution. 50:92-102.
Gerber, M.A. and L.R. Griffen. 2003. Inheritance and natural selection on functional traits. International Journal of Plant Science. 164:S21-S42.
Gilbert, M., N. Pammenter and B. Ripley. 2008. The growth responses of coastal dune species are determined by nutrient limitation and sand burial. Oecologia. 156:169-178.
Gilbert, M.E. and B.S. Ripley. 2008. Biomass reallocation and the mobilization of leaf resources support dune plant growth after sand burial. Physiology Plantarum. 134:464-472.
Hancock, T. and P. Hosier. 2003. Ecology of the threatened species Amaranthus pumilus Rafinesque. Castanea. 68:236-244.
Hesp, P.A. 1991. Ecological processes and plant adaptations on coastal dunes. Journal of Arid Environments. 21:165-191.
Intergovernmental Panel on Climate Change (IPCC). 2007. Climate Change 2007: Synthesis Report.
Ishikawa, S., S. Furukawa and T. Oikawa. 1996. Photosynthetic responses to drought conditions in three coastal dune plants in relation to their zonal distribution. Australian Journal of Botany. 44:381-391.
Ishikawa, S., T. Oikawa and S. Furukawa. 1990. Photosynthetic characteristics and water use efficiency of three coastal dune plants. Ecological Research. 5:377- 391.
Ishikawa, S., T. Oikawa and S. Furukawa. 1991. Responses of photosynthesis, leaf conductance and growth the different salinities in three coastal dune plants. Ecological Research. 6:217-226.
Johnson, D.M., M.J. Germino and W.K. Smith. 2004. Abiotic factors limiting photosynthesis in Abies lasiocarpa and Picea engelmannii seedlings below and above the alpine timberline. Tree Physiology. 24:377-386.
Korner, C. 1991. Some often overlooked plant characteristics as determinants of plant growth: a reconsideration. Functional ecology. 5:162-173.
Lambers, H., E.S. Chapin III and T.L. Pons. 1998. Plant Physiological Ecology. Springer Publishers, New York, NY (USA).
Larcher, W. 1995. Physiological Plant Ecology (3rd edition). Springer, Berlin (DEU).
144
Lechowicz, M.J. and P.A. Blais. 1988. Assessing the contributions of multiple interacting traits to plant reproductive success: environmental dependence.
Lee, J.A. and R. Ignaciuk. 1985. The physiolgocial ecology of strandline plants. Vegetatio. 62:319-326.
MacDonald, J. H. 2008. Handbook of Biological Statistics. Sparky House Publishing, New York, NY (USA).
Maun, M., R. Boyd, L. Olson. 1990. The biological flora of coastal dunes and wetlands. I. Cakile edentula (Bigel.) Hook. Journal of Coastal Research. 6:137-156.
Mooney, H.A., C. Field, W.E. Williams, J.A. Berry and O. Bjorkman. 1983. Photosynthetic characteristics of plants of a California cool coastal environment. Oecologia. 57:38-42.
Nilsen, E.T., T.T. Lei and S.W. Semones. 2009. Presence of understory shrubs constrains carbon gain in sunflecks by advance-regeneration seedlings: evidence from Quercus rubra seedlings growing in understory forest patches with or without evergreen shrubs present. International Journal of Plant Science. 170:735-747.
Nobel, P.S. 1999. Physiochemical and environmental plant physiology (2nd edition). Academic Press, New York, NY (USA).
Norman, G.R.N. and D.L. Streiner. 2000. Biostatistics: the bare essentials. B.C. Decker Publishers, London (GRB).
Oguchi, R., K. Hikosaka, T. Hiura and T. Hirose. 2008. Costs and benefits of photosynthetic light acclimation by tree seedlings in response to gap formation. Oecologia. 155:665-675.
Osmond, C.B., M.P. Austin, J.A. Berry, W.D. Billings, J.S. Boyer, J.W.H. Dacey, P.S. Nobel, S.D. Smith and W.E. Winner. 1987. Stress physiology and the distribution of plants. Bioscience. 37:38-48.
Oosting, H.J. 1945. Tolerance to salt spray of plants of coastal dunes. Ecology. 26:85- 89.
Papdi, C., M.P. Joseph, I.P. Salamo, S. Vidal and L. Szabados. 2009. Genetic technologies for the identification of plant genes controlling environmental stress responses. Functional Plant Biology. 36:696-720
Pearcy, R.W., O. Bjorkman, M.M. Caldwell, J.E. Keeley, R.K. Monson and B.R. Strain. 1987. Bioscience. 37:21-29.
145
Perumal, V.J. and M.A. Maun. 2006. Ecophysiological response of dune species to experimental burial under field and controlled conditions. Plant Ecology. 184:89-104.
Pilkey, O.H. and L. Pilkey-Jarvis. 2007. Useless arithmetic: why environmental scientists can’t predict the future. Columbia University Press, New York, NY (USA).
Quero, J.L., R. Villar, T. Maranon, R. Zamora, D. Vega and L. Sack. 2008. Relating leaf photosynthetic rate to whole-plant growth: drought and shade effects on seedlings of four Quercus species. Functional Plant Biology. 35:725-737.
Radford, A.E., H.E. Ahles and C.R. Bell. 1968. Manual of the Vascular Flora of the Carolinas. The University of North Carolina Press. Chapel Hill, North Carolina (USA).
Reich, P.B., D.S. Falster, D.S. Ellsworth, I.J. Wright, M. Westoby, J. Oleksyn and T.D. Lee. 2009. Controls on declining carbon balance with leaf age among ten woody species in Australian woodland: do leaves have zero daily net carbon balances when they die? New Phytologist. 183:153-166.
Reich, P.B., I.J. Wright, J. Cavender-Bares, J.M. Craine, J. Oleksyn, M. Westoby and M.B. Walters. 2003. The evolution of plant functional variation: traits, spectra, and strategies. International Journal of Plant Science. 164:S143-S164.
Reinhardt, K., D.M. Johnson and W.K. Smith. 2009. Age-class differences in shoot photosynthesis and water relations of Fraser fir (Abies fraseri), southern Appalachian Mountains, USA. Canadian Journal of Forest Research. 39:193- 197.
Russell, R.B., T.T. Lei and E.T. Nilsen. 2009. Freezing induced leaf movements and their potential implications to early spring carbon gain: Rhododendron maximum as exemplar. Functional ecology. 23:463-471.
Salisbury, F.B. and C.W. Ross. 1992. Plant Physiology (4th edition). Wadsworth Publishing Company, Belmont, CA (USA).
Sanders, H.L. 1968. Benthic diversity: a comparative study. American Naturalist. 102:243-282.
Schoenbaum, T.J. 1982. Islands, Capes, and Sounds. John F. Blair publisher, Winston- Salem, NC (USA).
Schulze, E.D., R.H. Robichaux, J. Grace, P.W. Rundel and J.R. Ehleringer. 1987. Plant water balance. Bioscience. 37:30-37.
146
Shao, G., H.H. Shugart and B.P. Hayden. 1996. Functional classifications of coastal barrier island vegetation. Journal of Vegetation Science. 7:391-396.
Shipley, B., D.Vile, E. Garnier, I.J. Wright and H. Poorter. 2005. Functional linkages between leaf traits and net photosynthetic rate: reconciling empirical and mechanistic models. Functional Ecology. 19:602-615.
Smith, A.M. and M. Stitt. 2007. Coordination of carbon supply and plant growth. Plant, cell and environment. 1126-1148.
Solbrig, O.T. 1981. Studies on the population biology of the genus Viola. II. The effect of plant size on fitness in Viola sororia. Evolution. 35:1080-1093.
Stallman, D.A. 2004. Echoes of Topsail. Carlisle Printing, Sugarcreek, OH (USA).
Strand, A.E. 2002. Characterization of the genetic structure in Amaranthus pumilus. Annual Report of the Department of Biology, College of Charleston, South Carolina (USA).
United States Fish and Wildlife Service. 1993. Endangered and threatened wildlife and plants; Amaranthus pumilus (seabeach amaranth) determined to be threatened. Federal Register 58(65): 18035-18041.
Weakley, A. and M. Bucher. 1992. Status survey of seabeach amaranth (Amaranthus pumilus Rafinesque) in North and South Carolina. Report to the North Carolina Plant Conservation Program, and Endangered Species Field Office, North Carolina.
Xiao, X, F. Yang, S. Zhang, H. Korpelainen and C. Li. 2009. Physiological and proteomic responses of two contrasting Populus cathayana populations to drought stress. Physiologia Plantarum. 136:150-168.
Yaun, T., M.A. Maun and W.G. Hopkins. 1993. Effects of sand accretion on photosynthesis, leaf-water potential and morphology of two dune grasses. Functional Ecology. 7:676-682.
Zhang, S.B., H. Hu and Z.R. Li. 2008. Variation of photosynthetic capacity with leaf age in an alpine orchid, Cypripedium flavum. Acta Physiol Plant. 30:381-388.
147
-2 -1 Table V-1. Total assimilation (mol CO2 m day ) for Amaranthus pumilus, Cakile edentula, Hydrocotyle bonariensis and Iva imbricata during representative days from June 2002 until May 2003. * denotes estimated assimilation.
Month A. pumilus C. edentula H. bonariensis I. imbricata 21 June (2002) 0.29 0.20 0.21 0.33
3 July 0.41 0.45 0.17 0.36
12 August 0.49 --- 0.29 0.37
17 September 0.12 --- 0.27 0.43
21 October --- 0.09 0.07 0.09
26 November --- 0.15 0.11 0.12
17 December --- 0.14 0.10 0.12
15 January (2003) --- 0.13 ------
4 February --- 0.08 ------
23 March --- 0.32 0.12* ---
17 April --- 0.18 0.14 0.18
20 May 0.74 0.54 0.45 0.62
148
-2 -1 Table V-2. Total monthly assimilation (mol CO2 m month ) for Amaranthus pumilus, Cakile edentula, Hydrocotyle bonariensis and Iva imbricata from June 2002 until May 2003. Total monthly assimilation was calculated by multiplying the total daily assimilation times the number of days in a particular month. * denotes estimated assimilation.
Month A. pumilus C. edentula H. bonariensis I. imbricata June (2002) 8.70 6.00 6.30 9.90
July 12.71 13.95 5.27 11.16
August 15.19 --- 8.99 11.47
September 3.60 --- 8.10 12.90
October --- 2.79 2.17 2.79
November --- 4.50 3.30 3.60
December --- 4.34 3.10 3.72
January (2003) --- 4.03 ------
February --- 2.24 ------
March --- 9.92 3.72* ---
April --- 5.40 4.20 5.40
May 22.94 16.74 13.95 19.22
Yearly Total 63.14 69.91 59.10 80.16 -2 -1 (mol CO2 m yr )
149
Table V-3. Best-fit equations for the photosynthetic light response of A. pumilus, C. edentula, H. bonariensis and I. imbricata.
Species Best-fit Equation r value p value
A. pumilus y = 1.33x X 10-2 + 8.66 X 10-1 0.87 p<0.001
C. edentula y = 6.13x X 10-3 + 8.85 X 10-1 0.68 p<0.001
H. bonariensis y = -2.24x2 X 10-6 + 8.36x X 10-3 + 6.53 X 10-1 0.60 p<0.001
I. imbricata y = 1.32x X 10-2 + 1.68 0.68 p<0.001
150 cloud cover
2500
2000 12 August 2002 -2 150 0 PAR A = 48.76 mol m -2 PART = 57.37 mol m 10 0 0 15% reduction due to cloud cover 500
0 48121620 SOLAR TIME (hrs X 100)
2500
PART 2000 26 November 2002 -2 PARA = 16.93 mol m 15 0 0 -2 PART = 28.40 mol m 1000 40% reduction due to cloud cover 500 0 4 8 12 16 2 0 SOLAR TIM E (hrs X 100)
2500
2000 )
23 March 2003 -1 -2 s PARA = 46.90 mol m -2 1500 PAR = 51.55 mol m-2 T m mol 9% reduction due to cloud 1000
cover ( PAR 500
0 4 8 12 16 20
SOLAR TIME (hrs X 100)
2500
29 June 2003 2000 )
-2 -1 PARA = 63.53 mol m s -2 -2 1500 PART = 64.50 mol m mol m mol
1.5% reduction due to cloud 1000 cover ( PAR 500
0 4 8 12 16 20 SOLAR TIME (hrs X 100)
Figure V-1. PAR measurements taken on representative days during 2002 and 2003. PARA = actual PAR, PART = theoretical PAR (red curve), % reduction due to clouds is also indicated.
151 30
21 JUN 2002 25
20
15
10
5
300
A. pumilus 3 JUL 2002 25 C. edentula H. bonariensis I. imbricata 20
15
10
5 ) -1 s -2 0 mol m mol 12 AUG 2002
A ( 25
20
15
10
5
0
17 SEP 2002 25
20
15
10
5
0 4 8 12 16 20 SOLAR TIME (hrs X 100)
Figure V-2a. Diurnal assimilation rates (A) taken once per month from June 2002 until September 2002. Bars indicate maximum standard error measured for each species.
152 30
21 OCT 2002 25
20
15
10
5
0
A. pumilus 26 NOV 2002 25 C. edentula H. bonariensis I. imbricata 20
15
10 ) -1 5 s -2 m 2 0 mol CO
17 DEC 2002 25 A (
20
15
10
5
0
15 JAN 2003 25
20
15
10
5
0 4 8 12 16 20 SOLAR TIME (hrs X 100)
Figure V-2b. Diurnal assimilation rates (A) taken once per month from October 2002 until January 2003. Bars indicate maximum standard error measured for each species.
153 30
4 FEB 2003 25
20
15
10
5
0
A. pumilus 23 MAR 2003 25 C. edentula H. bonariensis I. imbricata 20
15
10 ) 1 - 5 s 2 - m 2 0 mol CO
17 APR 2003 25 A (
20
15
10
5
0
20 MAY 2003 25
20
15
10
5
0 4 8 12 16 20 SOLAR TIME (hrs X 100)
Figure V-2c. Diurnal assimilation rates (A) taken once per month from February 2003 until May 2003. Bars indicate maximum standard error measured for each species.
154 30 Amaranthus pumilus 25
20
15
10
5
0 30 Cakile edentula 25
20
15
10 )
-1 5 s -2 m 2 0 30 mol CO mol
Hydrocotyle bonariensis 25 A (
20
15
10
5
0 30 Iva imbricata 25
20
15
10
5
0
0 200 400 600 800 1000 1200 1400 1600 1800 2000 PAR (mol m-2 s-1)
Figure V-3. Photosynthetic light response of Amarnathus pumilus, Cakile edentula, Hydrocoltyle bonariensis and Iva imbricata measured on 7 July 2002.
155
30 A 25
20
15
10 ) -1 s
-2 5 m 2
0 mol CO mol
A. pumilus, predicted PCG = 1.00, actual PCG = 0.44 B C. edentula, predicted PCG = 0.46, actual PCG = 0.52 A ( 25 H. bonariensis, predicted PCG = 0.36, actual PCG = 0.19 I. imbricata, predicted PCG = 1.00, actual PCG = 0.40 -2 -1 (Units are mol CO2 m day ) 20
15
10
5
0 4 8 12 16 20 SOLAR TIME (hrs X 100)
Figure V-4. Predicted (A) and actual (B) photosynthetic carbon gain (PCG) for Amaranthus pumilus, Cakile edentula, Hydrocotyle bonariensis and Iva imbricata.
156
1o dune
foredunes ocean beach face driftline swale Site 3 Site 1 Site 2 Site
Location 6/17/04 7/14/04 8/11/04 9/4/04
Site 1 44 33 26 10
Site 2 44 43 42 0
Site 3 44 42 41 0
Figure V-5. Schematic diagram of the three Amaranthus pumilus transplantation sites on Topsail Island, NC. The table insert depicts the number of plants surviving during each observation period.
157
30
Driftline Foredune 25 Primary dune Natural )
-1 20 s -2 m 2 15 mol CO 10 A (
5
0 4 8 12 16 20
SOLAR TIME (hrs X 100)
Figure V-6. Diurnal photosynthesis for representative Amaranthus pumilus plants at each of the transplantation sites as well as individuals found naturally growing in the driftline and foredune habitats. Measurements were taken on 14 July 2004.
158
) ) -2 -2 m m 2
2 PCG threshold PCG threshold (8 mol CO (20 mol CO Seedling Pre-reproductive Reproductive Seed Bank Stage Stage Stage Senesence
Maintenance -2 -1 (12 mol CO2 m month )
late Apr - early May June July late Sep - early Nov
Figure V-7. Conceptual model of how photosynthetic carbon gain (PCG) thresholds could relate to life-history stages in Amaranthus pumilus.
159
30
saltwater inundated 25 non-inundated )
-1 20 s -2 m 2 15 mol CO 10 A (
5
0 0 200 400 600 800 1000 1200 1400 1600 1800 2000
-2 -1 PAR (mol m s )
Figure V-8. Photosynthetic light response of Amaranthus pumilus plants both inundated and non-inundated with saltwater during a 9 July 2004 overwash event on Topsail Island, NC (A.G. Snow unpublished data).
160
Photosynthetic Species Carbon Gain (PCG) Fitness
Environmental Stress Filter
PCG PCG Potential Realized PCG PCG
SOLAR TIME SOLAR TIME
PCG loss PCG
SOLAR TIME
Figure V-9. Conceptual model of barrier island beach abiotic stresses, species response, and resultant PCG.
161
STRESSES Daily Seasonal Episodic
ORGANISM Physiology Life-History Leaf Anatomy RESPONSE Patterns and Orientation
COMMON Photosynthetic Allocation CURRENCY Carbon Gain Patterns (PCG)
Fitness
Figure V-10. Idealized relationship between abiotic stresses, plant response, PCG, allocation patterns and fitness in the barrier beach environment.
162 CHAPTER VI
CONCLUSIONS AND PREDICTIONS FOR THE FUTURE OF FOUR BARRIER
ISLAND BEACH PLANT SPECIES
This dissertation has reviewed relevant barrier beach plant ecology and
physiological plant ecology research (Chapter II) identifying a rich, historical record of
plant ecology studies from the West Coast (USA), East Coast (USA), Great Lakes (USA)
and Canada, but revealing a lack of studies applying ecophysiological techniques to
plants living in the barrier island (BI) beach environment. The objective of this
dissertation was to incorporate the tools of physiological ecology into an ecological study
that investigated the response of Amaranthus pumilus, Cakile edentula, Hydrocotyle
bonariensis and Iva imbricata, four plant species representing different functional groups,
to daily, seasonal and episodic stresses present on the coastal barrier island of Topsail
Island, NC.
Chapter III examined leaf form and function in relation to the model proposed by
Smith et al. (1997). Abaxial and adaxial stomatal frequencies, internal leaf anatomy and
the photosynthetic response to incident sunlight on the abaxial and adaxial leaf surfaces were measured. In general, leaves of A. pumilus, C. edentula, H. bonariensis and I. imbricata fit model predictions for a stressful environment with some exceptions.
Chapter IV addressed the importance of water stress and plant response in the BI beach environment. It was determined that water availability may be greater than previously thought, challenging the assumption that plants living in this environment are constantly
163 under water stress. None of the plants examined experienced xylem water potentials low enough to be considered very stressful. Each of the species demonstrated physiological and life-history attributes that likely maximized photosynthetic carbon gain over a given year, albeit via different combinations of traits. Chapter V explored the use of photosynthetic carbon gain (PCG) as a common currency when addressing species response to and ultimately fitness in the BI beach environment. Photosynthetic carbon gain was found to be potentially the most efficient single parameter in which to assess plant fitness/success in the BI beach environment. Total yearly PCG for A. pumilus, C. edentula, H. bonariensis and I. imbricata did vary and there appeared to be a threshold amount of carbon that each plant must assimilate in order to complete its life cycle. This carbon threshold could be related to functional group traits (structural/maintenance requirements). Conceptual models were presented that relate PCG reductions due to abiotic stresses, plant response to these stresses and overall impacts on plant fitness.
This dissertation has so far focused on historic plant ecology and ecophysiology studies relevant to East Coast (USA) BIs and response of A. pumilus, C. edentula, H. bonariensis and I. imbricata to the present BI beach environment. The remainder of this chapter will explore likely alterations to the BI beach environment due to climate change and possible ramifications for the future of these four plant species.
The Dynamic Nature of Barrier Islands section in Chapter II discussed future sea- level rise, increases in storm intensity and frequency and possible impacts upon BI beach organisms due to climate change. Because of their intimate association with the ocean,
BI beaches are predicted to experience climate change impacts more quickly and intensely than almost any other environment (Gilman et al. 2008, Wu et al. 2009). This
164 coupled with the unprecedented population migration to coastal areas over the past three
decades (Brown and McLachlan 2002) puts extreme pressure on BI beach habitats and
the organisms living within them.
Several studies have indicated that anthropogenic response to climate change
(especially sea-level rise) is of equal or more importance than the environmental factors
themselves (Crawford 2008, Dugan et al. 2008). “Hard” structures, such as groins, jetties
and seawalls, used to mitigate erosion caused by sea-level rise and storms have been
known for years to cause destruction and eventual loss of the beach - or an adjacent beach
(Pikley et al. 1998, Pilkey and Pikley-Jarvis 2008). Due to lessons learned, hard
structures are illegal in some states (Schoenbaum 1982) although “soft” structures such as
sand fences and sand bags are allowed. Planting vegetation to stabilize dunes is
successful in some instances (Woodhouse 1978), but is ineffective if storm surge of an
Extreme Episodic Storm Event (EESE) reaches a critical value (Roman and Nordstrom
1988, Feagin 2008, Koch et al. 2009).
Beach renourishment is an increasingly popular method to slow erosion but is expensive, requires continual sand inputs and negatively impacts flora and fauna
(Peterson and Bishop 2005 and references therein). Sea-level has fluctuated throughout the millenia and organisms that live at the land-sea interface have often been able to migrate seaward or landward with their habitat (Dolan et al. 1980, Ehrenfeld 1990,
Gilman et al. 2008). If humans continue to alter coastlines and reduce their dynamic nature, habitats and therefore organisms will not have the opportunity to relocate and extinction rates will likely rise (Feagin et al. 2005, Greaver and Sternberg 2007, Dungan et al. 2008). One promising development is the Coastal Barrier Island Network, a
165 recently funded (National Science Foundation) diverse group of biologists, geologists,
engineers, economists and sociologists that have begun to work toward a national policy
that promotes sustainable preservation, conservation and development of BI ecosystems within the natural limits imposed by a highly dynamic environment (Feagin et al. 2009)
Of the four species examined in this dissertation, A. pumilus is likely to be most negatively effected. Amaranthus pumilus was federally listed as threatened in 1993 due to extirpation from 75% of its historic range (US Fish and Wildlife Service 1993). This decline in range was mostly attributed to habitat loss due to development and hardening of the shoreline (Weakley and Bucher 1992). Amaranthus pumilus is a pioneering species that predominates in the driftline habitat of the barrier beach. Dispersal of seeds via overwash events and subsequent ocean currents carry A. pumilus to “zones of suitable habitat” which are usually accreting ends of BIs (Hancock and Hosier 2003). Due to climate change and anthropogenic factors, the future availability of such zones appears to be bleak.
Cakile edentula is a cool-weather annual found in lacustrine environments (Great
Lakes) as well as marine environments of the East and West Coast of the United States
(Barbour and Rodman 1970). The plant has a unique strategy for reproduction in that there is a proximal and distal seed for each fruit (Maun et al. 1990). The distal seed breaks off and is dispersed via ocean currents to new habitats while the proximal seed remains in place and is often buried with the parent plant. This strategy allows some seed to be distributed to new, potentially suitable habitats while some seed stays in the current, presumably suitable habitat. These, as well as other, characteristics may account for the
166 current extensive range of C. edentula. Future barrier beach habitat loss is likely to impact this species, but to a lesser extend that A. pumilus.
Hydrocotyle bonariensis grows on most barrier beaches of the Southeastern
United States (Evans 1988). This species not only inhabits the foredune and primary dune, but can also be found on secondary, tertiary (etc.) dunes and throughout slacks.
The greatest asset of H. bonariensis is probably its asexual growth via rhizomes. These rhizomes facilitate translocation of nutrients and water promoting resource acquisition in a heterogenous environment (Evans 1988, Evans 1991). This growth pattern, along with other functional traits, will probably allow H. bonariensis to fare better than A. pumilus in the barrier beach environment of the future. In one example illustrating this idea, Fahrig et al. (1993) found that plants with a clonal growth form recovered/recolonized BI beaches more quickly than other growth forms following an overwash event.
Of the four species examined in this dissertation, I. imbricata, is the only one producing substantial above ground, perennial growth (wood). Iva imbricata can be found along the coasts of southern Virginia to the Florida Keys, Gulf Coast of the United
States and on beaches of Caribbean Islands (Jackson 1960). On Topsail Island, NC (and other sandy BI beaches), I. imbricata defines the permanent vegetation line (i.e. foredune). For example, I. imbricata seedlings are found in the driftline, foredune and primary dune throughout the growing season. Winter storms, however, remove all vegetation up to a certain distance from the ocean. Iva imbricata seedlings that are not overwashed and removed survive into the next growing season (producing wood) and thereby define the line of permanent vegetation for the next year. Iva imbricata, therefore, is an excellent indicator of sea-level rise. Little attention has been paid to this
167 species in the past, but intensive studies documenting the seaward/landward migration and subsequent health of individual plants as well as populations would pay rich dividends concerning our knowledge of the effects (and status) of sea-level rise on BI beaches.
Figure VI-1 shows the effects of a seasonal overwash event on the driftline habitat of Topsail Island, NC. Notice that all of the driftline vegetation has been removed, but that the foredune vegetation (2nd, 3rd, etc. year growth of I. imbricata) remains – defining the line of permanent vegetation. Hydrocotyle bonariensis grows inland of this location and C. edentula is not usually present during this time of year. This overwash event effectively ended the growing/reproductive season of A. pumilus. What happens if storms such as this arrive earlier in the growing season? What happens as sea-level rises?
What happens if storms become more intense and more frequent? Will this drive A. pumilus to extinction? Will C. edentula, H. bonariensis and I. imbricata be adversely affected? Future research should be directed to answer these questions.
Literature Cited
Barbour, M.G. and J.E. Rodman. 1970. Saga of the West Coast sea-rockets: Cakile edentula ssp. californica and C. maritima. Rhodora. 72:370-386.
Brown, A.C. and A. McLachlan. 2002. Sandy shore ecosystems and the threats facing them: some predictions for the year 2025. Environmental Conservation. 29:62- 72.
Crawford, R.M.M. 2008. Plants at the margin. Cambridge University Press, Cambridge (GBR).
Dolan, R., B. Hayden and H. Lins. 1980. Barrier islands. American Scientist. 68:16-25.
Dungan, J.E., D.M. Hubbard, I.F. Rodil, D.L. Revell and S. Schroeter. 2008. Ecological effects of coastal armoring on sandy beaches. Marine Ecology. 29:160-170.
Ehrenfeld, J.G. 1990. Dynamics and processes of barrier island vegetation. Aquatic
168 Sciences. 2:437-480.
Evans, J.P. 1988. Nitrogen translocation in a clonal dune perennial, Hydrocotyle bonariensis. Oecologia. 77:64-68.
Evans, J.P. 1991. The effect of resource integration on fitness related traits in a clonal dune perennial, Hydrocotyle bonariensis. Oecologia. 86:268-275.
Fahrig, L., B. Hayden and R. Dolen. 1993. Distribution of barrier island plants in relation to overwash disturbance: a test of life history theory. Journal of Coastal Research. 9:403-142.
Feagin, R.A. 2008. Vegetation’s role in coastal protection. Science. 320:176-177.
Feagin, R.A., D.J. Sherman and W.E. Grant. 2005. Coastal erosion, global sea-level rise, and the loss of sand dune plant habitats. Frontiers in Ecology and the Environment. 3:359-364.
Feagin, R.A., W.K. Smith, N.P. Psuty, D.R. Young, J.C. Gibeaut, M.L. Martinez, K.F. Nordstrom, N.L. Jackson, G.A. Carter, J.N. Gemma, R.E. Koske, D.H. Thomas, J.C. Whitehead and K.L. Lucas. 2009. Barrier islands: coupling anthropogenic stability with ecological sustainability. Journal of Coastal Research (in press).
Gilman, E.L., J. Ellison, N.C. Duke and C. Field. 2007. Threats to mangroves from climate change and adaptation options: a review. Aquatic Botany. 89:237-250.
Greaver, T.L. and L.S.L. Sternberg. 2007. Fluctuating deposition of ocean water drives plant function on coastal sand dunes. Global Change Biology. 13:216-223.
Hancock, T.E. and P.E. Hosier. 2003. The ecology of seabeach amaranth (Amaranthus pumilus Rafinesque). Castanea. 68:236-244.
Jackson, R.C. 1960. A revision of the genus Iva L. University of Kansas Science Bulletin. 41:793-896.
Koch, E.W., E.B. Barbir, B.R. Silliman, D.J. Reed, G.M.E. Perillo, S.D. Hacker, E.F. Granek, J.H. Primavera, N. Muthiga, S. Polasky, B.S. Halpern, C.J. Kennedy, C.V. Kappel and E. Wolanski. 2009. Non-linearity in ecosystem services: temporal and spatial variability in coastal protection. Frontiers in Ecology and the Environment. 7:29-37.
Maun, M.A., R.S. Boyd and L. Olson. 1990. The biological flora of coastal dunes and wetlands. 1. Cakile edentula (Bigelow) Hooker. Journal of Coastal Research. 6:137-156.
Peterson, C.H. and M.J. Bishop. 2005. Assessing the environmental impacts of beach
169 nourishment. BioScience. 55:887-896.
Pilkey, O.H., W.J. Neal, S.R. Riggs, C.A. Welsh, D.M. Bush, D.F. Pilkey, J. Bullock and B.A. Cowan. 1998. The North Carolina Shore and Its Barrier Islands: Restless Ribbons of Sand. Duke University Press, Durham, NC (USA).
Pilkey, O.H. and L. Pilkey-Jarvis. 2007. Useless Arithmetic: Why Environmental Scientists Can’t Predict the Future. Columbia University Press, New York, NY (USA).
Roman, C.T. and K.F. Nordstrom. 1988. The effect of erosion rate on vegetation patterns of an East Coast barrier island. Estuarine, Coastal and Shelf Science. 26:233-242.
Schoenbaum, T.J. 1982. Islands, Capes, and Sounds. John F. Blair publisher, Winston- Salem, NC (USA).
Smith, W.K., T.C. Vogelmann, E.H. DeLucia, D.T. Bell and K.A. Shepherd. 1997. Leaf form and photosynthesis. Bioscience. 47:785-793.
United States Fish and Wildlife Service. 1993. Endangered and threatened wildlife and plants; Amaranthus pumilus (seabeach amaranth) determined to be threatened. Federal Register 58(65):18035-18041.
Weakley, A.S. and M.A. Bucher. 1992. Status survey of seabeach amaranth (Amaranthus pumilus Rafinesque) in North and South Carolina. Report to the North Carolina Plant Conservation Program and Endangered Species Field Office, North Carolina (USA).
Woodhouse, Jr. W.W. 1978. Dune building and stabilization with vegetation. Special Report Number 3. United States Army Corps of Engineering Coastal Research Center. Fort Belvoir, Virginia (USA).
Wu, S.Y., R. Najjar and J. Siewert. 2007. Potential impacts of sea-level rise on the Mid- and Upper-Atlantic region of the United States. Climatic Change. 95:121-138.
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driftline foredune
Figure VI-1. Southwestern end of Topsail Island, NC before (6 August 2001) and after (6 October 2001) a storm overwash event. Notice that all driftline vegetation has been removed, but that foredune vegetation (2nd, 3rd, etc. year growth of Iva imbricata) remains – defining the permanent line of vegetation.
171 THOMAS E. HANCOCK [email protected] 336-408-5927
EDUCATION
Doctor of Philosophy (biology) Wake Forest University, 2009 Advisor: William K. Smith
Master of Science (marine biology) University of North Carolina at Wilmington, 1995 Advisor: Paul H. Hosier
Bachelor of Science (biology) University of North Carolina at Charlotte, 1993
Continuing Education AP Physics Summer Institute, University of Alabama AP Biology Summer Institute, Stanford University AP Biology Summer Institute, North Carolina State University Integrating Zoological Parks into the High School Curriculum, Bronx Zoo NY
PUBLICATIONS
W. K. Smith, C. R. Brodersen, T.E. Hancock and D.M. Johnson. 2004. Integrating plant temperature measurement using heat-sensitive paint and color image analysis. Functional Ecology. 18:148-153.
W. K. Smith, M. J. Germino, T. E. Hancock, and D.M. Johnson. 2003. A more unified approach for interpreting elevational limits of upper timberlines. Tree Physiology. 23:1101-1112.
Hancock, T.E. and P.E. Hosier. 2003. Ecology of the Threatened Species Seabeach Amaranth (Amaranthus pumilus Rafinesque). Castanea. 68:236-244.
Hackney, C.T., S. Brady, L. Stemmy, M. Boris, C. Dennis, T. Hancock, M. O’Bryon, C. Tilton, and E. Barbee. 1996. Does intertidal vegetation indicate specific soil and hydrologic conditions. Wetlands. 16:89-94.
172 PRESENTATIONS
2008. Plant strategies for mediating water stress in a North Carolina (USA) barrier beach environment. Oral presentation. Association of Southeastern Biologists annual meeting.
2008. Response of plant species to periodic and episodic stresses on a North Carolina (USA) barrier beach. Oral presentation. Wake Forest University.
2003. Adaptation to daily, annual, and episodic stressors in barrier beach plants. Oral presentation. North Carolina Academy of Science annual meeting.
2002. Species living on the edge: ecophysiological adaptation to episodic events, climate change, and biodiversity in barrier island beach plants. Oral presentation. Ecological Society of America annual meeting.
2002. Species living on the edge: ecophysiology and survival of Cakile edentula (C3), Hydrocotyle bonariensis (C3) and the threatened Amaranthus pumilus (C4) on a North Carolina (USA) barrier island. Oral presentation. Association of Southeastern Biologists annual meeting.
1996. Ecology of the Threatened Species Seabeach Amaranth (Amaranthus pumilus Rafinesque). Poster presentation. Association of Southeastern Biologists annual meeting.
GRANTS
2004. Vecellio Award. Wake Forest University. $1250.
2003. Vecellio Award. Wake Forest University. $900.
2002. Core Student Award. Southern Appalachian Botanical Society. $200.
1993-1995. Ecology of the Threatened Species Seabeach Amaranth (Amaranthus pumilus). Northeast New Hanover County Conservancy. $3,000.
PROFESSIONAL ORGANIZATIONS
Ecological Society of America Association of Southeastern Biologists Southern Appalachian Botanical Society North Carolina Academy of Science North Carolina Science Teachers Association
173 WORK EXPERIENCE
Director of Conservation Bald Head Island Conservancy September 2009 - present
Biology Instructor Alamance Community College January – September 2009
Visiting Instructor of Biology Salem College February 2008 – January 2009
Science Department Chairperson Bishop McGuinness Catholic High School August 2005 - February 2006, November 2006 - February 2008
Science Teacher Bishop McGuinness Catholic High School August 2003 - February 2006, November 2006 - February 2008
Officer in Charge Current Operations Division Joint Intelligence Group Joint Task Force Guantanamo Bay, Cuba February – October 2006
Research Assistant/Teaching Assistant Wake Forest University January 2001 - August 2003
Minister of Youth Main Street Baptist Church March 2001 - August 2003
Coordinator of Marketing and Development Carolina Biological Supply Company October 1999 - March 2001
AP Biology Product Manager Carolina Biological Supply Company February 1999 - October 1999
174 Technologist Carolina Biological Supply Company February 1998 - February 1999
Science Teacher Guilford County Schools February 1996 - February 1998
Research Assistant/Lab Coordinator Center for Marine Science Research (UNC Wilmington) September 1995 - February 1996
Teaching Assistant/Research Assistant UNC Wilmington August 1993 - September 1995
MILITARY
Intelligence Officer Navy Reserve 2nd Fleet, Norfolk VA February 2002 – present
Seaman Navy Reserve Triad Armed Forces Reserve Center, Greensboro NC February 2000 – February 2002
INTERESTS/SKILLS
Reader for Advanced Placement (AP) Biology Exams Commercial Drivers’ License (B) North Carolina Zoological Society North Carolina Coastal Federation Soccer coach for girls U10 recreation
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