Viscin Cells in the Dwarf Mistletoe Arceuthobium ... - Davidsonia

Volume 17, Number 3 

July 2006 

Davidsonia 

A Journal of Botanical Garden Science

Davidsonia 

Editor 

Iain E.P. Taylor 

UBC Botanical Garden and Centre for Plant Research 

University of British Columbia 

6804 Southwest Marine Drive 

Vancouver, British Columbia, Canada, V6T 1Z4 

Editorial Advisory Board 

Quentin Cronk 

Fred R. Ganders 

Daniel J. Hinkley 

Carolyn Jones 

Lyn Noble 

Murray Isman 

David Tarrant 

Roy L. Taylor 

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Pam Sinclair 

Associate Editors 

Mary Berbee (Mycology/Bryology) 

Moya Drummond (Copy) 

Aleteia Greenwood (Art) 

Michael Hawkes (Systematics) 

Richard Hebda (Systematics) 

Douglas Justice (Systematics and Horticulture) 

Eric La Fountaine (Publication) 

Jim Pojar (Systematics) 

Andrew Riseman (Horticulture) 

Charles Sale (Finance) 

Janet R. Stein Taylor (Phycology) 

Sylvia Taylor (Copy) 

Roy Turkington (Ecology) 

Jeannette Whitton (Systematics) 

Davidsonia is published quarterly by the Botanical Garden of the University 

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ISSN 0045-09739 

Cover: The Arceuthobium americanum fruit, seed, and viscin tissue. Mature recurved fruit 

photographed two days prior to explosive discharge. Photo: Cynthia M. Ross 

Back Cover: UBC graduate students mark off transects for ecological field 

study. Photo: Esson et al.

Davidsonia 17:3 73 

Editorial 

This issue of Davidsonia (I apologize that it is regrettably late again) 

contains the next in the series of papers about the Garry oak ecosystem. 

The authors (Esson et al.) are graduate students in the UBC Botany 

Department and the results presented in this paper were collected during 

the annual UBC Botany Department graduate student field trip. 

Participation in this field trip is compulsory for every graduate student, 

usually during their first year of study in the department. Periodically, 

either the teaching faculty or the students question the relevance of this 

brief field experience. The argument is that students who do not plan 

to work in the field can spend their time more profitably pursuing their 

laboratory research plans. A broader argument is that botany has changed 

and only those pursuing research in systematics and ecology need this 

field experience. 

At the same time, the cries continue for more knowledge about the 

natural history of plants that can be used by those who work to address 

the effects of climate change and biodiversity loss due to urbanization or 

other human activities. The irony is that some of the needed information 

is already available but languishes in the thesis chapters that are deemed to 

be unsuitable for publication in the modern high-profile research journals. 

Fortunately some journals, such as Rhodora, Madroño, and Davidsonia, 

continue to publish scientific natural history with some of the reassurance 

about quality that comes from peer-review. In addition, much excellent 

natural history is increasingly available on internet web sites. 

The political decision makers who are responsible for national 

policy on biodiversity loss or the botanical impacts of climate change 

expect scientific answers to be available on demand. There are fewer 

university researchers who are active in natural history than there were 20 

or more years ago. One benefit is that the alarms over biodiversity loss 

have drawn many evolutionary biologists closer to the field. Those doing 

the undoubtedly important research to understand the genetic (and hence 

evolutionary) relationships among organisms seem to have an operating 

Iain E.P. Taylor, Professor of Botany and Research Director, 

UBC Botanical Garden and Centre for Plant Research, 

6804 SW Marine Drive, Vancouver, BC, Canada, V6T 1Z4. 

iain.taylor@ubc.ca

74 

principle that high publication rate is a diagnostic sign of competence, 

and is to be rewarded by substantial research funding. Given the reality 

of limited research funding, the slower projects are poorly funded, indeed 

such slow-progressing scholars may be deemed unsuitable for a tenured 

position. The result is that long-term study on life-history or resolution 

of several physical forms in a single life history (larva-adult invertebrates; 

anamorph-teleomorph fungi) has become ‘side project’ research and even 

when the work is done, the necessary taxonomic expertise and herbarium 

facilities are limited or in some cases no longer available. 

The question remains, “Where are we to find future generations of 

scientific naturalists” As the biodiversity loss and climate change alarm 

bells ring louder, students will certainly see the need and the opportunity 

to strengthen and even reconstruct the foundation of natural history 

scholarship upon which we have relied up to now. How many species 

remain to be discovered, catalogued and systematically assessed The 

estimates vary widely but the numbers are very large, particularly in nonvascular 

plant, microbial and invertebrate biology. Clearly, we must meet 

the need for competent expert observation and understanding of the 

principles of taxonomy, regardless of whose taxonomic philosophy one 

may prefer. But fieldwork requires substantial funding to cover travel 

costs to and from research sites; costs of personal living on site; and 

preparation of herbarium and museum material, data processing, and 

continuing costs associated with ensuring the research specimens 

are stored properly and space can expand to contain the vital 

new materials. The field station, usually funded from charitable trusts 

or endowments, has itself become an endangered institution, especially if 

funding has come from an institution’s main budget allocation. Botanical 

gardens may already have picked up some of the natural history obligations, 

but those who are lucky enough to do research at these places have an 

increasing obligation to take a much more proactive role in leading the 

resurrection of scientific natural history. Many of my generation (students 

in the 1950s) link their decision to become field biologists directly to a 

well organized, albeit short, excursion to study plants in their natural 

setting.


Viscin Cells in the Dwarf Mistletoe 

Arceuthobium americanum — 

“Green Springs” with Potential Roles in 

Explosive Seed Discharge 

and Seed Adhesion 

Abstract 

The genus Arceuthobium comprises angiosperms that are aerial parasites on 

Pinaceae and Cupressaceae. These parasites are serious forest pests in North 

America, where they damage timber trees. Arceuthobium spreads by explosive 

discharge, which is facilitated by a sticky fruit tissue called “viscin” that remains 

on the dispersed seed and enables its adhesion to the next host. Viscin tissue 

is comprised of mucilaginous, elongated viscin cells. The purpose of this 

study was to further characterize the viscin cells. Arceuthobium americanum (the 

lodgepole pine dwarf mistletoe) has viscin cells that have spirally-arranged cell 

wall fibrils. These cellular “springs” are shorter within the fruit than when 

outside and hydrated, which suggests that their expansion results from a pressure 

release that aids in propulsion. Following drying, viscin cells again coil and 

shorten, securing the seed to the host. Discharged viscin cells contain green 

chloroplasts and show a positive reaction for operation of oxidation-reduction 

biochemistry when stained with tetrazolium chloride, indicative of viability. 

Introduction 

The genus Arceuthobium (the dwarf mistletoes; family Viscaceae) 

is a group of new and old world dioecious angiosperms that are 

aerial parasites on Pinaceae and Cupressaceae (Hawksworth and 

Wiens 1996). These parasites are economically important in Canada, 

especially in British Columbia (BC) and Alberta, where they are 

destructive pathogens of commercially valuable coniferous timber trees 

(Hawksworth 1983). Arceuthobium infection causes annual economic 

losses amounting to an estimated 3.8 x 10 6 m 3 of lumber in western 

Cynthia M. Ross, Assistant Professor, 

Department of Biological Sciences, Thompson Rivers University, 

P.O. Box 3010, 900 McGill Rd., Kamloops, BC, Canada, V2C 5N3. 

cross@tru.ca

76 

Canada (Hawksworth and Wiens 1996). Results of tree disease include 

the formation of host branch clumps called “witches’ brooms,” dieback, 

reduced growth, a compromised lifespan, and curtailed reproduction 

as well as increased susceptibility to other diseases and injury (Geils 

and Vázquez Collazo 2002). While Dendroctonus ponderosae (the mountain 

pine beetle) has gained much notoriety as a serious forest problem in 

BC, infection by Arceuthobium is widespread and has been implicated 

in the predisposition of trees to beetle attack (Johnson et al. 1976; 

McGregor 1978; McCambridge et al. 1982). Of the forest pathogens 

causing mortality in natural conifer systems, Arceuthobium is perhaps one 

of the most significant (Winder and Shamoun 2006). 

Ecologically, the implications of Arceuthobium infection are complex: 

these mistletoes are influential symbionts that affect numerous aspects of 

population genetics and coevolution (Geils and Vázquez Collazo 2002). 

It is thought that the presence of Arceuthobium in a stand significantly 

increases habitat diversity. As such, the role of Arceuthobium in natural 

conifer systems has often clashed with human interests and harvesting 

practices (Shamoun et al. 2003). However, with an understanding of the 

ecology and biology of Arceuthobium and their hosts, wiser management 

practices may follow. 

Arceuthobium spreads solely by seed, which is discharged explosively 

from mature fruit at the end of the growing season (Hawksworth and 

Wiens 1996). A seed can be dispersed as far as 20 m from its source plant. 

Viscin tissue is a unique mucilaginous region that forms a layer around 

the embryo-pole of the single seed within each fruit. The extracellular 

hygroscopic mucilage imbibes water during fruit development 

(Hawksworth and Wiens 1996; Ross 2002) and provides the hydrostatic 

force needed for explosive discharge. Following discharge, the viscin 

tissue remains around the dispersed seed and facilitates its adherence to 

any surface the seed may strike, including its next host. 

Several studies on the general development and chemistry of the 

tissue include one by Paquet et al. (1986), who described the tissue 

as being comprised of elongated “viscin cells” that secrete a largely 

pectinaceous mucilage. These authors also found that the viscin cells 

of discharged seeds could be wetted and dried several times before the 

mucilage was washed away. Gedalovich-Shedletzky et al. (1989) noted 

that viscin cell development begins as slightly elongated parenchyma 

in the carpellary region and that the non-pectic monosaccharides,


xylose and glucose, were also present in the mucilage. However, other 

features of the viscin cells, such as their cell walls, have not been well 

characterized. My small study on aspects of the viscin cells not directly 

related to the mucilage has shown that viscin cells seem to function in 

discharge and remain viable enough to function in adhesion to new host 

sites. The post discharge fate of the viscin cells has not been described, 

but chloroplasts were present, and the cells tested positively for the 

operation of oxidation-reduction biochemistry when stained with 

tetrazolium chloride. As seed is the only means by which Arceuthobium 

can spread, an understanding of seed development and dispersal may 

provide the basis for an effective control program. 

Methods 

Collection and Observation of Fruit and Viscin Cells Prior 

to Explosive Discharge 

At least 30 pistillate aerial shoots of Arceuthobium americanum (the 

lodgepole pine dwarf mistletoe) containing mature fruit were marked in 

the field and each was enclosed in cheesecloth on August 20, 2005. The 

contents of the cheesecloth bags were sampled daily until September 2, 

2005 (the day on which explosive discharge occurred) then 1 day, 3 days 

and 10 days following discharge. Samples from each shoot were fixed 

immediately in 2% paraformaldehyde + 2% glutaraldehyde in a 0.1 M 

phosphate buffer (pH 6.8), kept at 4 °C overnight, rinsed in the same 

buffer, and postfixed with 2% osmium tetroxide in the same buffer for 

4 hours. The material was dehydrated in an ethanol series and embedded 

in Spurr’s resin (Spurr 1969). Sections (2 µm thick) were obtained using 

a Sorvall Porter-Blum JB-4 microtome (Sorvall, Newtown, Connecticut) 

and affixed to gelatin-coated glass slides (Jensen 1962). The slides were 

stained with 2% crystal violet in a 0.05 M ammonium oxalate buffer 

(pH 6.7) and were observed and photographed with a Nikon Optiphot 

compound light microscope (Nikon, Tokyo, Japan). 

Within-fruit viscin cell lengths were measured using a micrometer slide 

calibrated to an eyepiece scale. Average viscin cell length was determined 

by measuring the 10 most apical viscin cells (i.e., those cells proximal to the 

embryo and stigma, distal to the pedicel) in sections from 10 fruits sampled 

on September 1, 2005 (the day in 2005 prior to explosive discharge).

78 

Collection and Observation of Seeds and Viscin Cells 

Following Explosive Discharge 

In the lab, at least 10 seeds per sample date were removed from 

the cheesecloth with forceps, wetted, placed on glass plates, and 

photographed with an Olympus SZH DFplan dissecting microscope 

(Olympus, Tokyo, Japan). Those same seeds were allowed to dry on the 

glass plates overnight, and were photographed again. Whole mounts 

of both wet and dry viscin cells were made and photographed with 

the Nikon Optiphot compound light microscope. Measurements of 

outside-fruit viscin cell lengths were obtained as before for both the wet 

and dried viscin cells for each of the three seed collection dates. 

Viability of the viscin cells was assessed using 5 seeds picked off the 

cheesecloth wraps on each of the three collection dates. Seeds were 

presoaked in distilled water for 24 hours, placed into sterile Petri plates, 

and submerged in 1% (w/v) 2,3,5-triphenyl tetrazolium chloride (2,3,5- 

TTC) in the dark for 72 hours (Scharpf and Parmeter 1962). The staining 

reaction of the viscin cells was examined at the light microscope level. 

Red staining indicated operation of oxidation-reduction biochemistry, a 

sign of viability. 

Results and Discussion 

The mature fruit, which was bicoloured and recurved (Figure 1), 

contained a single seed consisting of an embryo and endosperm 

enveloped in a conspicuous uniseriate layer of mucilaginous viscin cells 

(Figure 2). The viscin tissue surrounded three-quarters of the embryocontaining 

apical region of the seed, i.e., the embryo-pole. 

Rehydrated seeds collected from the cheesecloth 1, 3, and 5 days 

following explosive discharge had the same general appearance (Figure 3). 

Discharged seeds with the viscin tissue layer were, on average, 2.5 mm 

long. The viscin cells were green and contained chloroplasts that were 

visible under the compound microscope (Figure 4). While chloroplasts 

have been observed in the endosperm and embryo of Arceuthobium species 

(Hawksworth and Wiens 1996), this is the first report of chloroplasts in 

the viscin cells of any mistletoe. If they are functional, they may have 

a biosynthetic role during the early stages of parasite connection to the 

host. The cellulose fibrils of the viscin cell walls had a distinct helical 

arrangement (Figure 4), which unlike elaters of fern sporangia (Mauseth


Image: Cynthia M. Ross 

Figure 1. The Arceuthobium americanum fruit, seed, and viscin tissue. Mature recurved fruit 

photographed two days prior to explosive discharge. scale bar = 4 mm. 

1988), involved a spiral coiling of the cellulose fibrils of the primary 

cell wall along the long axis of the cell. This has not been previously 

described in any other plant cells and requires further study. 

The resemblance of these viscin cells to “springs” may reflect a 

function in explosive seed discharge, adhesion, or both. The elaters 

of fern sporangia are helical cells with a role in spore discharge but the

80 


Figure 2. Longitudinal section through mature fruit; same orientation as in Figure 3. 

Evident within the fruit is the embryo and endosperm of the seed, as well as the 

uniseriate layer of elongated, mucilaginous viscin cells. 

en = endosperm; ey = embryo; v = viscin cells; scale bar = 360 µm



Figure 3. A whole hydrated seed collected from cheesecloth the day after explosive 

discharge. The relative position of the embryo, endosperm, and viscin cells are 

indicated; note the green colour of the viscin cells. 

en = endosperm; ey = embryo; v = viscin cells; scale bar = 420 µm 

mechanism relies on tension due to drying rather than an accumulation 

of hydrostatic pressure. The “springs” are oriented in a way that could 

allow uncoiling to push the seed free from the fruit upon release of 

pressure.

82 


Figure 4. Whole hydrated viscin cells obtained from a seed collected the day following 

explosive discharge; note the helically-arranged cellulose fibrils of the viscin cell 

walls as well as the obvious green chloroplast. c = chloroplast; scale bar = 50 µm 

Support for this role of viscin cells in discharge comes from 

comparison of viscin cell lengths within the mature fruit (780 µm ± 20 

µm) with the lengths of rehydrated viscin cells outside of the fruit (860 

µm ± 20 µm). This measurement was consistent regardless of the time 

of seed collection. The energy released from the uncoiling of the spring 

could have been used to aid propulsion. While the overall increase in 

viscin cell length is relatively small (average 10%), approximately 1,000 

viscin cells comprise the viscin tissue, and so their collective expansion 

might be significant. 

Roth (1959) noted that most seeds initially encounter and stick to 

host needles; the first autumn rain then wets the mucilage and, if the 

seed had been intercepted by an upright needle, gravity pulls the welllubricated 

seed to the needle base where penetration can eventually 

occur. As needles constitute the largest target area, this mechanism 

would greatly increase the efficiency of dispersal; the fact that the viscin


cell mucilage can endure repeated wetting and drying (Paquet et al. 

1986) provides support for such a mechanism. Further characterization 

of the viscin cell mucilage is required to gain an understanding of the 

biochemistry behind this phenomenon. When a seed becomes lodged 

at a needle base and is no longer capable of rehydration, the viscin cells 

may also function to tether the seed to the host in an orientation that 

places the embryo in the most effective position for infection. Firstly, 

as the viscin cells and associated mucilage are located at the embryo- 


Figure 5. A whole seed collected the day after explosive discharge; the seed was 

allowed to dry onto a glass plate (the embryo was dissected out of the seed for 

photographic purposes only). 

en = endosperm; ey = embryo; v = viscin cells.; scale bar = 570 µm

84 


Figure 6. Whole viscin cells obtained from a seed collected 10 days following explosive 

discharge and stained with 2,3,5-triphenyl tetrazolium chloridescale (2,3,5-TTC). 

Note the obviously red-stained nucleus, which is viable. n = nucleus; bar = 50 µm 

pole, the embryo will be drawn into close contact with the host when 

the mucilage permanently dries. Secondly, the viscin cell helical walls 

recoil upon drying; when whole seeds were dried on glass plates, the 

viscin cells shortened and the coiling became visibly tighter, anchoring 

the seed downward (Figure 5). 

Viscin cell functions outside the fruit may depend on their biochemical 

activity. Scharpf and Parmeter (1962) examined the viability of the 

Arceuthobium embryos with the vital oxidation-reduction stain 2,3,5- 

triphenyl tetrazolium chloride (2,3,5-TTC). We observed evidence of


such activity in the viscin cells. Examination with the light microscope 

showed that nuclei stained red and were thus showing some signs of 

viability (Figure 6). 

I have shown that the viscin cells of Arceuthobium are specialized 

and unique, and have structural potential for roles in seed discharge 

and adhesion. The presence of chloroplasts as well as observation 

of biochemical activity in viscin cells following discharge need to 

be investigated further, as viscin cells could perhaps be involved in 

photosynthesis and even host recognition. A better understanding of 

seed discharge and primary colonization of a new host may prove to be 

valuable in future management of Arceuthobium parasitism. 

Acknowledgements 

I wish to thank Thompson Rivers University (TRU) for funding provided 

by a Scholarly Activity Grant, as well as the Natural Sciences and Engineering 

Research Council (NSERC) of Canada for a Discovery Grant I was 

awarded at TRU. I also thank my former Ph.D. supervisor, Dr. Michael 

J. Sumner, for his support and encouragement in my academic endeavors. 

References 

Gedalovich-Shedletzky, E., Delmer, D., and Kuijt, J. 1989. Chemical composition 

of viscin mucilage from three mistletoe species – a comparison. Annals 

of Botany 64: 249-252. 

Geils, B.W., and Vázquez Collazo, I. 2002. Loranthaceae and Viscaceae in North 

America. In Mistletoes of North American Conifers. Technical Coordinators, 

B.W. Geils, J. Cibrián Tovar, and B. Moody. United States Department 

of Agriculture, Forest Service, Rocky Mountain Research Station, General 

Technical Report RMRS-CTR-98. pp. 1-8. 

Hawksworth, F.G. 1983. Mistletoes as Forest Parasites. In The Biology of 

Mistletoes. Edited by D.M. Calder and P. Bernhardt. Academic Press, 

New York. pp. 317-333. 

Hawksworth, F.G., and Wiens, D. 1996. Dwarf mistletoes: biology, pathology, 

and systematics. United States Department of Agriculture, Forest Service, 

Agricultural Handbook 709. 

Jensen, W.A. 1962. Botanical histochemistry: principles and practice. San 

Francisco, CA: W.H. Freeman & Company.

86 

Johnson, D.W., Yarger, L.C., Minnemeyer, C.D., and Pace, V.E. 1976. Dwarf 

mistletoe as a predisposing factor for mountain pine beetle attack of 

ponderosa pine in the Colorado Front Range. United States Department 

of Agriculture, Forest Service, Rocky Mountain Region, Forest Insect 

and Disease Management, Technical Report R2-4. 

Mauseth, J.D. 1988. Plant anatomy. Menlo Park, CA: The Benjamin/Cummings 

Publishing Company, Inc. 

McCambridge, W.F., Hawksworth, F.G., Edminster, C.B., and Laut, J.G. 1982. 

Ponderosa pine mortality resulting from a mountain pine beetle outbreak. 

Department of Agriculture, Forest Service, Rocky Mountain Forest and 

Range Experiment Station, Research Paper RM-235. 

McGregor, M.D. 1978. Management of Mountain Pine Beetle in Lodgepole 

Pine Stands in the Rocky Mountain Area. In Theory and Practice of 

Mountain Pine Beetle Management in Lodegpole Pine Forests. Edited by 

A.A. Berryman, G.D. Amman, R.W. Stark, D. Kibbee, and S. Hieb. 

Moscow, ID: University of Idaho Press. pp. 129-139. 

Paquet, P.J., Knutson, D.M., Tinnin, R.O., and Tocher, R.D. 1986. Characteristics 

of viscin from the seeds of dwarf mistletoe. Botanical Gazette 

147: 156-158. 

Rödl, T., and Ward, D. 2002. Host recognition in a desert mistletoe: early stages 

of development are influenced by substrate and host origin. Functional 

Ecology 16: 128-134. 

Ross, C.M. 2002. Development of the female flowers and fruit in the dwarf 

mistletoe Arceuthobium americanum (Viscaceae). Ph.D. thesis. Department 

of Botany, University of Manitoba, Winnipeg, MB. 

Roth, L.F. 1959. Natural emplacement of dwarf mistletoe seed on ponderosa 

pine. Forest Science 5: 365-369. 

Shamoun, S.F., Ramsfield, T.D., and van der Kamp, B.J. 2003. Biological control 

approach for management of dwarf mistletoe. New Zealand Journal of 

Forestry Science 33: 373-384. 

Scharpf, R.F., and Parmeter, J.R. 1962. The collection, storage, and germination 

of seeds of a dwarf mistletoe. Journal of Forestry 60: 551-552. 

Spurr, A.R. 1969. A low viscosity epoxy resin embedding medium for electron 

microscopy. Journal of Ultrastructural Research 26: 31-43. 

Winder, R.S., and Shamoun, S.F. 2006. Forest pathogens: friends or foe to 

biodiversity Canadian Journal of Plant Pathology 28:S221-S227.


Comparison of Two Garry Oak Sites 

Undergoing Restoration on Southeastern 

Vancouver Island: a Preliminary Study 

ABSTRACT 

Garry oak ecosystems represent unique species-rich communities in the Pacific 

Northwest United States and southwestern Canada. These distinct ecosystems 

are becoming rare as their integrity is threatened by urban and agricultural encroachments, 

as well as by the introduction of non-native plant taxa. We visited 

two Garry oak parklands, one that had been heavily impacted until recently 

by grazing cattle, and one that has been protected from such anthropogenic 

activities for several years and currently has an active restoration program. 

We compared the quantitative occurrence and compositional variation of six 

regionally common plant species between these two sites using univariate and 

multivariate statistical methods. Our results showed clear differences in the 

quantitative patterns of abundance and overall variation among species between 

the two sites. These results indicate that the restoration efforts at Site 2 have 

promoted greater coverage of native species and greater community variation, 

both considered to be positive indicators of biodiversity for this ecosystem. 

INTRODUCTION 

Garry oak (Quercus garryana) ecosystems occur in the northwestern 

United States from the Puget Trough in Washington State, to low 

elevations in the Klamath Mountains on the Oregon/California 

border (Natureserve, 2006). The Canadian sites that are found along 

the southeastern coast of Vancouver Island and throughout the Gulf 

Islands, are at the northern limits of the ecosystem (Dunn and Ewing, 

1997). These Garry oak communities are thought to be remnants of a 

hardwood forest that covered much of the Pacific Northwest between 

ice ages. Garry oak communities reached their widest distribution 

Heather Esson, Aaron Heiss, Chris Sears* and Nyssa Temmel, 

Graduate Students, Department of Botany, 

University of British Columbia, Vancouver, BC, V6T 1Z4. 

All authors contributed equally. 

*Author for correspondence: e-mail: sears@interchange.ubc.ca

88 

approximately 6000 years ago during the Holocene period, when the 

region experienced a warmer and dryer climate than at present (Allen 

et al. 1999). When the coastal climate changed to the wetter and cooler 

weather that we experience today, the hardwood ecosystems were outcompeted 

by conifers in many areas. Garry oaks and their associated 

plant communities persisted in Canada on rapidly draining soils present 

on steep south and west facing slopes, and on dryer sites with exposed 

bedrock and periodic fires (Erickson, 1993). 

Prior to European settlement ca. 150 years ago First Nations people 

harvested plants (e.g. Camassia quamash and Allium acuminatum) and 

deer (Odocoileus hemionus) from Garry oak savannas. To help maintain 

these valuable resources they periodically burned them to prevent 

encroachment from conifers and to promote food and forage species 

(Turner, 1999). Today, less then 5% of pre-European Garry oak 

savannas remain in British Columbia. This is primarily due to historical 

and recent urban and agricultural development. Furthermore, Garry 

oak ecosystems are threatened by invasive species that are believed to 

out-compete native taxa (Erickson, 1993). Approximately 100 plant 

and animal species are “at risk” in these systems, including 23 species 

that have been designated as threatened or endangered throughout their 

global range (GOERT, 2006). Given that the future of these ecosystems 

in Canada are in jeopardy, many community and scientific organizations 

are involved in conservation efforts. Some of these efforts involve 

protection from cattle grazing and reintroducing native species to 

meadows that have lost some of their original compliment of species. 

Garry oak ecosystems exhibit higher levels of biodiversity than most 

other ecosystems in western Canada (MacDougall, 2004). Biodiversity 

can be viewed as the variety of information contained in any biological 

community (Noss, 1990). For example, a population of a given species 

with high allelic variation would have high genetic biodiversity; a species 

with many subspecies would have high species biodiversity; and an 

ecosystem with a great variety of species represented would have high 

ecosystem biodiversity. Our brief ecological survey investigated one 

aspect of this latter type of biodiversity relating to changes in the overall 

patterns of distribution and abundance of six plant species that are 

characteristic of Garry oak communities.


Photo: Esson et al. 

Figure 1. Sample site 1 at Somenos Garry Oak Protected Area, April 26 th , 2005. 

The general purpose of our study was to assess the extent to 

which Garry oak systems were influenced by agriculture and urban 

development by comparing a heavily disturbed site to a site that had 

been placed under protection and had a rehabilitation program in place. 

Specifically, we addressed the following two questions: (1) did the 

quantitative occurrence of a representative group of six plant species 

differ significantly between the two sites, and (2) did the two sites differ 

in their biodiversity information as expressed through the patterns of 

assemblages among the six species 

METHODS 

In late April 2005, we conducted a vegetation survey at two Garry oak 

parkland sites, which we visited during a University of British Columbia 

Botany Graduate Field Course. Site 1 was in the Somenos Garry Oak 

Reserve, and was adjacent to a new housing development (Figure 1).

90 

This site was considered to be highly anthropogenically affected as the 

area has been used for livestock grazing and recreational activities for 

many years, and has had the native topsoil removed from large areas. 

The oaks were logged during the early 1940s to provide thwarts for 

Mosquito fighter planes needed for Canada’s war effort (A. MacDougall, 

2006, personal communication). The only rehabilitation method 

for Site 1 has been recent exclusion of agricultural ungulates. Site 2 

was the Cowichan Garry Oak Reserve that is located on land used as 

grazing pasture between 1880 and 1980. At the time of the study the 

land was protected from grazing and an active program was underway 

to reestablish a number of native Garry oak savanna plant species 

(Figure 2). 

As our time for field sampling at the two sites was limited, we focused 

our study on six species including an abundant invasive grass (Dactylis 

glomerata), and five native perennial forbs (Camassia quamash, Sanicula 

crassicaulis, Ranunculus occidentalis, Dodecatheon hendersonii and Lomatium 

utriculatum). The five native species were chosen because they were 


Figure 2. Sample site 2 on reclaimed farmland, April 26 th , 2005.



Figure 3. Camassia quamash, Dodecatheon hendersonii and Ranunculus occidentalis. 

commonly present in current Garry oak meadow plant assemblages, 

which facilitated comparisons between the sites. Further, we assumed 

these regionally common species to be surrogates for the overall 

responses of native and exotic species to the various changes affecting 

this system (e.g. intense herbivory, fire suppression, invasive plants, etc.). 

Figures 3 and 4 show some of the more charismatic flowering plants we 

encountered during our survey. 

We ran replicate 60 m transects parallel to the prevailing slopes at the 

two sites and placed 1 m 2 quadrats at 0, 20, 40, and 60 m so as to capture 

as much variation as possible in the vegetation at each site. We recorded 

the orientation of each transect using a compass and made sure that each 

quadrat was placed squarely with the transect line running through the 

middle. Within each quadrat we visually estimated the percent coverage 

of each of the six plant species using the Braun Blanquet cover scale 

(1 =

92 

Photos: Esson et al. 

Figure 4. Some of the herbaceous native flora observed in the Garry oak meadows 

visited, clockwise from upper left: Dodecatheon hendersonii, Erythronium oregonum, 

Orobanche uniflora, and Fritillaria lanceolata.


Based on purely subjective observations, we noted that there appeared 

to be more grass coverage at Site 1 than at Site 2. Lomatium utriculatum 

was only recorded at the second site. For general comparison, we visited 

a less disturbed site at a Garry oak savanna located on the west side of 

Mt. Tzuhalem. It seemed to contain many more native plant species 

and in greater abundance, but we did not sample in this area due to the 

fragile nature of this site. 

We used analysis of variance (ANOVA) to compare mean percent 

cover values and the grass forb/ratio between sites and used a posthoc 

Bonferroni adjustment to test if the means significantly differed 

between the sites (p

94 

the second site (Figure 5). It is interesting to note that when all six 

transects from Site 2 were included in the PCA the area enclosed by the 

confidence ellipses remained largely unchanged. The difference in areas 

enclosed within the confidence ellipses, and their degree of separation, 

indicate that the patterns of assemblages of plant species differ between 

the two sites. 

DISCUSSION 

Are there implications regarding biodiversity and 

prioritizing restoration projects 

The two sites differed significantly in the quantitative occurrence 

of four of the six species and the grass/forb ratio. Camasia quamash 

is known to be a “fair to good graze for sheep and cattle” (USDA, 

1937). This may account for the relative rarity of this taxon at Site 1 

Variable Site 1 Site 2 

DAGL 1.69 (1.62) 2.25 (1.48) 

CAQU* 0.375 (1.08) 1.94 (1.12) 

SACR 2.06 (1.77) 1.25 (1.57) 

RAOC* 0.125 (0.5) 1.19 (1.47) 

DOHE* 0.187 (0.54) 1.25 (1.39) 

LOUT* 0 (0) 1.06 (1.34) 

GF* 2.25 (2.18) 1.48 (0.95) 

Table 1: Mean cover scale values for Dactylis glomerata (DAGL), Camassia quamash 

(CAQU), Sanicula crassicaulis (SACR), Ranunculus occidentalis (RAOC), Dodecatheon 

hendersonii (DOHE) and Lomatium utriculatum (LOUT) and grass/forb ratio (GF) for 

two Garry oak communities on southern Vancouver Island. Standard deviations 

appear in parenthesis. An * denotes means which differed significantly (p < 0.05) 

between sites.


Figure 5: Scatterplot of scores on principal component 1 (PC 1) vs. PC 2 from a 

PCA of cover scale values for Sanicula crassicaulis, Dactylis glomerata, Lomatium utriculatum, 

Camassia quamash, Ranunculus occidentalis, Dodecatheon hendersonii, Sanicula crassicaulis 

and grass/forb ratios at two Gary oak communities on southern Vancouver Island. 

Ellipses enclose 68% of samples within a group. Values in parenthesis indicate 

percent variation explained by component.. 

compared to Site 2 as the latter had excluded agricultural ruminants for 

a longer period of time, perhaps giving this population time to increase 

its density. A greater grass/forb ratio at Site 1 relative to Site 2 (Table 1) 

implies that invasive plant taxa comprised a greater part of the flora at 

Site 1 than at Site 2 as invasive Bromus spp. and Dactylis glomerata were 

a large component of the grass flora at these sites. A site with high 

biodiversity is generally to be preferred over one with low biodiversity, 

particularly if that biodiversity is in the form of native species. Invasive 

species tend not to have the allelic variation inherent to natives due to 

founder effects (Lande, 1988) and can also demonstrate more plasticity 

in resource use and therefore fewer novel adaptations (Kolar and 

Lodge, 2001) so biodiversity is often a good measurement of priority 

for selection, should the conservationist need to choose between any

96 

two abiotically similar sites. Biodiversity carries profound implications 

for conservation. Biological information, once lost, is irretrievable. 

The highest priorities for conservation vary according to a number of 

criteria, but the amount of biological information in the systems under 

consideration is almost always one of them. 

Grass/forb ratio and Camasia quamash cover had the greatest influence 

along PC 1 of the PCA scatterplot (Figure 5). PC 1 accounted for 33% 

of variation in the data set and represents variation between sites. PC 2 

describes variation within sites. Intra-site variation was greatest in Site 2 

as indicated by the greater area enclosed by the 1 standard deviation 

confidence ellipse. Taken together these results suggest that Site 2 not 

only has a greater native component to its flora but also has more robust 

populations of native taxa than Site 1. As there is an association between 

decreasing numbers of indigenous species present and invasion of nonnative 

species, the introduction of non-native species to an area can be 

responsible for a reduction in biodiversity (Myers and Bazely, 2003). 

The prospect of ecological restoration inherently carries the promise 

of positive change in biodiversity, in particular the reduction of invasive 

species and the re-establishment of native species (Packard and Mutel, 

2005). 

To return to the question posed at the outset: are there implications 

regarding biodiversity and prioritizing restoration projects The answer 

is a political one: “Some, but not very much.” From a species-richness 

standpoint, we found that the quantitative occurrence of four of the 

six investigated species differed between sites and that the second site 

was marginally more diverse in patterns of plant species assemblages 

than the first. From the standpoint of conservation, the second site 

is preferable (although only slightly) as a starting point, which is not 

surprising, as it was originally somewhat less disturbed, is already under 

protection, and restoration efforts on it have already begun. 

ACKNOWLEDGEMENTS 

We thank Andrew MacDougall, now at the University of Guelph, for help in the 

field and with the manuscript. Corinne Cluis compiled the data. Gary Bradfield, 

Jack Maze, and Gina Choe kindly helped with the manuscript and statistical analysis.


REFERENCES 

Allen, G.B., Brown, K.J. and Hebda, R.J. 1999. Surface pollen spectra from 

southern Vancouver Island, British Columbia. Canadian Journal of 

Botany 77: 786-799. 

Dunn, P. and Ewing, K. 1997. Ecology and conservation of the South Puget 

Sound Prairie landscape. Seattle, Washington: The Nature Conservancy 

of Washington. 

Erickson, W. 1993. Garry Oak Ecosystems. Victoria BC: Wildlife Branch, BC 

Ministry of Environment, Lands and Parks. 

GOERT. 2006. Garry Oak Ecosystems Recovery Team [web application]. Victoria, 

BC. Canada. http://www.goert.ca/ (Accessed: October 16, 2006). 

Kolar, C.K. and Lodge, D.M. 2001. Progress in invasion biology: predicting 

invaders. Trends in Ecology and Evolution 16: 199-204. 

Lande, R. 1988. Genetics and demography in biological conservation. Science. 

241: 1455-1459. 

MacDougall, A.S. 2004. Joint effects of competition, recruitment limitation, 

and fire suppression in an invaded oak savanna ecosystem. PhD thesis, 

Department of Botany, University of British Columbia, Vancouver BC. 

Myers, J.H. and Bazely, D.R. 2003. Ecology and Control of Introduced Plants. 

Cambridge UK: Cambridge University Press. 

NatureServe. 2006. NatureServe Explorer: An online encyclopedia of life 

[web application]. Version 5.0. NatureServe, Arlington, Virginia. 

http://www.natureserve.org/explorer (Accessed: October 16, 2006 ). 

Noss, R.F. 1990. Indicators for monitoring biodiversity: A hierarchical approach. 

Conservation Biology. 4: 355-364. 

Packard, S. and Mutel, C.F. 2006. The Tallgrass Restoration Handbook 

for Prairies, Savannas, and Woodlands, 2 nd edition. Washington, D.C.: 

Island Press. 

Turner, N. J. 1999. “Time to burn:” Traditional use of fire to enhance resource 

production by aboriginal peoples in British Columbia. In Indians, fire 

and the land in the Pacific Northwest. Edited by R. Boyd. Oregon State 

University Press, Corvallis, OR. pp. 185-218. 

USDA. 1937. Range plant handbook United States Department of Agriculture, 

Forest Service. Washington, D.C. 532 p. 

SYSTAT. 2002. SYSTAT, version 10.2.01. SYSTAT Software Inc., Evanston, 

IL.

98 

Book Reviews 

Flowering and its manipulation 

edited by Charles Ainsworth 

volume 20 in the Annual Plant Reviews series, 

Blackwell Publishing (11 chapters, 285 pages). 

This handy book in the Annual Plant Reviews series is intended 

to be a convenient source of topical and up-to-date material on the 

biology of flowers and flowering for researchers and postgraduates. By 

and large, it succeeds. 

Part 1 covers “Core development and genetics” including floral 

induction and patterning. Part 2 covers “Specialized components of 

development” such as monoecy and cytoplasmic male sterility (CMS). 

Part 3 is curiously called “A developmental genetic model for the origin 

of the flower.” This must be a typographical error as this is the title 

of a stimulating chapter in the first part by Baum and Hileman. This 

part has nothing to do with the origin of the flower, but does contain 

useful chapters on flower colour and scent. A single chapter on flower 

senescence (appropriately the final chapter) is given a “part” of its own 

(Part 4). 

Baum and Hileman’s developmental genetic model for the 

evolutionary origin of the flower is one of the most interesting and 

innovative chapters in the book. Baum and Hileman propose a threestage 

model for the origin of the flower from a unisexual lax cone. 

The first step (according to them) is the evolution of a bisexual axis 

via a gynomonoecious intermediate. They speculate that homeotic 

conversion of microsporophylls to megasporophylls in a pollen cone is 

responsible, probably involving changes in the B-class and C-class floral 

MADS-box genes. 

Quentin Cronk, Professor of Plant Science and Director, 

UBC Botanical Garden and Centre for Plant Research, 

University of British Columbia, 6804 SW Marine Drive, 

Vancouver, BC, V6T 1Z4


The next step, they posit, is that the axis became compressed and 

determinate as C-class genes became negative regulators of the meristem 

gene, WUSCHEL. Then a petaloid perianth evolved by sterilization 

of the outer stamens. Baum and Hileman speculate that 

this arose by WUSCHEL evolving a reciprocal regulatory function 

for the C-class genes. Finally, a dimorphic perianth evolved (calyx 

and corolla). This, they suggest, coincides with B-class gene function 

becoming dependent on the expression of the gene UNUSUAL 

FLORAL ORGANS (UFO). This model is highly speculative, but as 

the authors point out, it fits the facts and makes testable predictions. 

Kramer (chapter 3) gives a very useful state-of-play review of floral 

patterning by MADS-box and other genes. The ABC model originally 

put forward by Coen and Meyerowitz 15 years ago has stood the test of 

time remarkably well. Elements have been added but the original core 

model has come through intact. As Kramer points out the more recently 

discovered E-class genes could not have been found by the original 

mutagenesis screens because of their high redundancy. However, our 

understanding still relies heavily on Arabidopsis and Antirrhinum. Further 

refinements will almost certainly come from the investigation of a wider 

range of flowering plants. 

Generally, the book is timely with excellent quality and good 

coverage of the subject. If I have one quibble it is with the references. 

Mostly these are fine. However three chapters (2, 4 and 5) 

unaccountably have no titles of articles in the references. This 

inconsistency makes it hard for the reader to judge the subject 

matter and relevance of this mysteriously title-less cited literature.

100 

Biology of the Plant Cuticle 

edited by Markus Riederer and Caroline Müller 

2006 

Blackwell Publishing. ISBN: 1-4051-3268-X 

The plant cuticle is the interface between the plant and its 

environment. Thus, its biological properties must reflect the important 

roles it plays in both biotic and abiotic interactions. Composed of both 

waxes and cutin, a bio-polyester the structure of which is still unknown, 

this multi-functional hydrophobic layer is the focus of intense research. 

This book presents a thorough and comprehensive review of this 

research covering every aspect of the biology of this important surface, 

the first of its kind in many years. Significant progress has been made 

in this field in recent years making the publication of this volume very 

timely. 

The introductory chapter provides a logical and succinct overview 

of the essential functions of the cuticle and serves as an introduction 

to the subsequent chapters. It also provides an extensive literature 

review of every function that has been attributed to the cuticle, briefly 

describing the supporting evidence that demonstrates the properties of 

the cuticle with respect to these functions. 

Chapter 2, nearly a book on its own, is a detailed analysis of the cuticle 

from the perspective of ultra microscopy technique. A careful review of 

the literature with descriptive figures and excellent micrographs provides 

an in depth analysis of the ontogeny and developmental aspects of the 

cuticle. In addition, the author provides extensive descriptions of the 

different structural kinds of cuticles that have been described as well 

as the distribution of these types within plants and plant organs. A 

similar extensive review of the morphology and distribution amongst 

plants of epicuticular wax types is also in this chapter. In short, this 

is perhaps the most extensive literature review of the ultrastructure of 

David Bird, Post Doctoral Fellow, 

Department of Botany, University of British Columbia, 

Vancouver, BC, V6T 1Z4


plant cuticles ever published. As a reference, it is invaluable, as it will 

serve as a comparative index of cuticle structures from a staggering 

number of plants. 

Cutin is a polyester, made up of monomers derived from C16 and 

C18 fatty acids. However, like many plant polymers such as lignin, 

the three dimensional structure of the assembled polymer is still a 

mystery. Chapter 3 is a succinct description of what is known about 

the properties and structure of the cutin biopolymer matrix. This 

chapter describes analytical techniques in polymer chemistry that are 

not familiar to the typical plant biologist, nevertheless, even a casual 

read provides an interesting overview of this fascinating polymer 

matrix. It is important to mention here that the authors do not lose 

sight of the biological relevance of the physico-chemical properties 

that have been described using advanced techniques such as solid state 

NMR. For example, the elasticity of tomato fruit cuticles is important 

to prevent fruit cracking, which is a costly disorder in tomato crops. 

Chapters 4 and 5 provide a careful review of the composition and 

biosynthesis of cuticular waxes, respectively. With a special emphasis 

on the experimental approaches used to determine these compositions, 

chapter 4 provides the reader not only with a very useful review of 

available methodologies, but also an extensive and critical examination 

of the current literature describing the composition of waxes in plants 

studied to date. The biosynthetic pathways responsible for the waxes 

are described in the subsequent chapter providing an extensive and upto-date 

review of the genes and enzymes involved in these pathways. 

As well, a thoughtful discussion on the little-understood secretion and 

transport of the waxes from the presumed site of biosynthesis to the 

plant surface is also provided. 

The optical properties of the plant surface are potentially important 

to the plant with respect to UV radiation. Chapter 6 describes the current 

methods available for studying surface optics with special reference to 

the plant cuticle. 

Chapters 7 and 8 describe the cuticle with respect to its permeability 

to both lipophyllic and polar compounds. The issue of transport across 

the cuticle is relevant to not only fundamental biological questions

102 

such as the release of defensive plant secondary metabolites, but also 

agricultural applications such as herbicide efficacy. These chapters 

provide an introduction to the approaches used by researchers in this 

field as well as useful literature reviews. 

The main physiological function of the cuticle is the prevention of 

water loss; the transpiration of water through the cuticle is the focus 

of chapter 9. Much of the literature describing the permeability of 

plant cuticles to water requires a good understanding of the theory that 

addresses the transport of water through a membrane. This chapter 

provides an explanation of these models and the application of them 

in describing the environmental effects on water transpiration through 

plant cuticles and the significance of stomatal closure with respect to 

water loss. 

In addition to its role in water relations, the cuticle is also important 

in post-embryonic development, being required for the prevention of 

organ fusion. The biological significance of the phenotypes of known 

cuticle mutants is discussed in Chapter 10. Special emphasis is made on 

the model plant Arabidopsis thaliana, where much of the recent advances 

in this area have been made. 

The role of the cuticle in the interactions between plants and 

microorganisms and insects is the focus of the last three chapters. Like 

the previous chapters, clear explanations of the methodologies, and 

their respective pros and cons, are provided in addition to a review of 

the state of knowledge in these fields. 

Biology of the Plant Cuticle is not only comprehensive in its content, 

but also the chapters are well integrated. Individual chapters do not 

stand alone, but refer to the other chapters where relevant. Moreover, 

an extensive index is provided as well. I would strongly recommend this 

text as an authoritative reference for anyone interested in this aspect of 

plant biology.


Gleanings 

Notes on papers (some technical and others less so) 

that caught the Editor’s eye 

Journal articles 

Studying the ethics of ecological restoration 

Vidra, R.L. 

2006 

Ecological Restoration 24: 100-101. 

The ethical challenges faced by ecological restorationists 

Dickinson, W. and 11 others. 

2006 


Developing a code of ethics for restorationists 

Carpenter, A. and 12 others. 

2006 


A short introduction and 2 papers written under the direction of 

Dr. Rebecca Vidra while she was teaching a science writing course 

to freshmen at Duke University. The papers by Dickinson et al. and 

Carpenter et al. are based on information obtained from surveys 

completed by members of the Society for Ecological Restoration 

International. Seven ethical dilemmas were reported, the most common 

being: conflicts between a client and what is right; sacrificing nature 

for financial gain; and withholding and/or falsifying data. The prime 

concerns for a code of ethics were that it should require sound science 

and avoid conflicts of interest. Respondents also felt strongly that 

religion, philosophy, and politics should be excluded from the code.

104 

The allure of meadow gardens 

Ottesen, C. 

May-June 2006 

The American Gardener 85 (3): 31-35. 

A short, clear and well-illustrated article that is based on the history of 

the meadow garden at American Horticultural Society headquarters in 

Alexandria, VA. The writer provides valuable advice on starting and 

maintaining a meadow garden and gives a firm reminder to “let it be”. 

Understory vegetation dynamics of 

North American boreal forests 

Hart, S.A. and Chen, H.Y.H. 

July 2006 

Critical Reviews in Plant Science 25: 381-397. 

A review with particular emphasis on recovery after disturbance 

by fire. The evidence shows that early recovery is characterized 

by high biodiversity, which decreases with time and is essentially 

stable after 40+ years. The paper looks at implications for forest 

management and really does review the situation rather than blinding 

the reader with gratuitous statistical re-analyses of data. 

Identification of potential organisms of relevance 

to Canadian boreal forest and northern lands 

for testing of contaminated soils 

Römbke, J., Jänsch, S., and Scroggins, R. 

2006 

Environmental Reviews 14 (2): 137-167. 

A review article that reminds readers of the importance of invertebrates 

in the biology of contaminated soils and their ecological restoration. 

While the details will be of value to invertebrate ecologists, the paper 

gives useful insight to the methods used in toxic soil restoration and the 

possibilities of finding, testing and eventually introducing invertebrates 

that can assist in the remediation processes.

Table of Contents 

Editorial 

Taylor 

Viscin Cells in the Dwarf Mistletoe 

Arceuthobium americanum — 

“Green Springs” with Potential Roles in Explosive 

Seed Discharge and Seed Adhesion 

Ross 

Comparison of Two Garry Oak Sites Undergoing 

Restoration on Southeastern Vancouver Island: 

a Preliminary Study 

Esson et al. 

Book Reviews 

Gleanings 

73 

75 

87 

98 

103

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