The Biology of Canadian Weeds: 157. Hedera Helix L. and Hedera

Canadian Journal of Plant Science

The Biology of Canadian Weeds. [#].Hedera helix L. and Hedera hibernica (G. Kirchn.) Bean

Journal: Canadian Journal of Plant Science ManuscriptFor ID CJPS-2018-0009.R1 Review Only Manuscript Type: Article

Date Submitted by the Author: 15-Feb-2018

Complete List of Authors: Strelau, Matthew; Trinity Western University, Biology Clements, David; Trinity Western University, Biology Benner, Jordan; Simon Fraser University Prasad, Raj; Natural Resources Canada, Pacific Forestry Centre; Retired Scientist, pacific forestry centre

Keywords: English ivy, Irish ivy, Hedera helix, Hedera hibernica, liana

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The Biology of Canadian Weeds. [#].Hedera helix L. and Hedera hibernica (G.

Kirchn.) Bean

M. Strelau1, D.R. Clements1, J. Benner2, and R. Prasad3

1Department of Biology, Trinity Western University, Langley, BC V2Y 1Y1 (e-mail:

[email protected])

2School of Resource and Environmental Management, Simon Fraser University, Burnaby, BC For ReviewV5A 1S6 Only 3Natural Resources Canada, Pacific Forestry Centre, 506 Burnside Rd., Victoria, BC, V8Z 1M5

Strelau, M., Clements D.R., Benner J. and Prasad R. 2017. The Biology of Canadian Weeds.

[#]. Hedera helix L. and Hedera Hibernica (G. Kirchn.) Bean. Can. J. Plant Sci. [#]: [] pp.

Two related species of Hedera spp. exist throughout Canada; English Ivy (Hedera helix) and

Irish Ivy (Hedera hibernica (G. Kirchn.) Bean). These species are difficult to distinguish

taxonomically and clear distinctions are not always made in the literature, so we largely discuss

them as a single taxon in this account. Ivy is an evergreen perennial with two distinct forms:

woody vine (juvenile form) or shrub (adult form). In Canada, Hedera spp. are found naturalized

along the southern coast of British Columbia (Vancouver, Vancouver Island, and Gulf Islands)

and in southwestern Ontario. During the past century, ivies have greatly expanded their ranges

along the Pacific and Atlantic coasts of North America, and in New Zealand, Australia, South

Africa, Brazil, and Hawaii. Ivy is physiologically plastic, invading both semiopen and deeply

shaded forests. It forms a dense ground cover that can inhibit native vegetation. It grows up tree

trunks and competes for soil nutrients, frequently leading to tree damage or even tree fall.

Invasive characteristics include evergreen habit, persistence, and vegetative reproductive

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capabilities. Humans have accelerated the spread of ivy by planting it along highway

embankments and medians to control soil erosion, and through widespread sale as an ornamental plant. There is debate among horticulturalists and ecologists over the destructive and

advantageous effects of ivy growth and sale within North America. Various methods of control

(chemical, manual, biological, and integrated) may be used to manage this species, but more

research is needed to design better control techniques.

Key Words: English ivy, Irish ivy, Hedera helix, Hedera hibernica, liana.

For Review Only

1. Names

I. Hedera helix L.; English ivy, common ivy, European ivy, ivy, Canary island ivy, Algerian ivy, lierre commun (Hausen 1987; Darbyshire et al. 2000; Metcalfe 2005). Bayer code: HEEHE

(Darbyshire et al. 2000).

II. Hedera hibernica hort. (syns. H. helix ssp. hibernica (Kirchener) Bean, H. helix var. hibernica

(McAllister and Rutherford 1990; Metcalfe 2005), H. helix ‘Hibernica’ and H. hibernica

‘Hibernica’ (Clarke et al. 2006)); Irish ivy.

Araliaceae, aralia family, ginseng family, ivy family, araliacées.

Araliaceae comprise 55 genera and 1500 species (Wen et al. 2001). There is a pronounced debate

over the classification and taxonomy of English ivy and its relatives. The genus Hedera

comprises 812 species from Eurasia (Wen et al. 2001) and approximately 16 taxa throughout

Europe, North Africa, Macaronesia, and Asia (Ackerfield and Wen 2003). Taxa within Asia and

Cyprus are not entirely defined (Ackerfield and Wen 2002). Additionally, there is a disagreement

over the classification of the genus Hedera and associated species such as H. helix (Ackerfield

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and Wen 2003). Contrary to the previous concept for its cladistic relationships, Wen et al. (2001)

discovered that Hedera is most closely related to the BrassaiopsisEuaraliopsisTrevesia clade

and related to Dendropanax. Wen et al. (2001) argue that morphology and intraspecific variation

suggest a need for careful taxonomic classification with additional datasets of Hedera. There is a

considerable lack of consensus over the taxonomy of Hedera spp., as indicated by the range from

one to six European Hedera spp. species recognized. Hedera hibernica is seen as a horticultural

form that is intermediate between H. helix ssp. helix and ssp. canariensis (Metcalfe 2005). There

is a range of classificationsFor for H. hibernicaReview with specialists Only using a variety of synonyms (e.g.

McAllister and Rutherford 1990; Metcalfe 2005; Clarke et al. 2006). Therefore, clearly

distinguishing between H. helix and H. hibernica is difficult. One survey in the Pacific

Northwest region of North America found that the majority of ivy sampled, previously thought

to be Hedera helix, was actually Hedera hibernica (Clarke et al. 2006). Clarke et al. (2006)

suggests that English ivy taxa are not as genetically differentiated as other plant groups. Lastly,

many botanists argue about the classification of ivy as either a liana or a vine, due to the thick

woody stem (Okerman 2000). Disagreements over phylogeny will require research into

traditional taxonomy (morphology), molecular taxonomy (DNA barcoding), and webbased

application tools that allow scientists to share and compare data (Kur et al. 2016).

2. Description and Account of Variation

(a) Physical description – Hedera sp. is a perennial evergreen with two distinct forms: a woody

vine to 30 m (juvenile form) or a shrub (adult form) to 2 m. Stems are creeping in the juvenile

form and have roots at leaf nodes with adventitious rootlets that have the ability to develop into

true roots. Rootlets range from 130 cm depending upon age and habitat and have no ability to

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absorb food or water. They occur on climbing vines approximately 510 cm below the apical

meristem, at nodes and along the internodes. Juvenile vines develop an alternate phyllotaxis, pubescent stems, and a heliotropic, climbing growth habit. In contrast, adult stems grow upright

and do not climb. Stems are purplegreen with internodes 46 cm long. Ivy rootlets secrete a

nanocomposite adhesive to climb up trees and other vertical structures (Xia et al. 2011). Leaves

are alternate, simple, coriaceous, exstipulate, evergreen, glabrous and dimorphic. Juvenile leaves

have 3 or 5 lobes (46 x 68 cm). The terminal lobe is as broad as long, while the two basal lobes

may be reduced or absent.For Wedgeshaped Review lobes are usually Only more prominent on leaves of

climbing stems. Leaf bases are cordate, with shallow sinuses and apices that are bluntly acute

with veins noticeably lighter in colour. Adult leaves are mostly unlobed (58 x 47 cm),

markedly narrower on shoots exposed to light and broader on those in the shade; their shape is

ovate to rhombic and the bases are shallowly cordate to cuneate (Fig. 1a); juvenile leaves are

lobed (Fig. 1b). Petioles on both the juvenile and adult leaves are about as long as the leaf.

Young shoots and leaves are glabrous. Leaves of flowering stems (610 cm) are entire, ovate, or

rhombic.

Flowers are hermaphroditic, actinomorphic in globose umbels, which may be solitary or grouped in a racemose panicle (Figs 1c and d; Fig. 2c). The inflorescence is umbellate and carries 1015 flowers, 57 mm across. The sepals (5) are persistent, very small, and fused at the base. Ovaries are 5celled and inferior; the top is a conical disk that has five alternate stamens with yellowish green petals, 35 mm long. The center of the disk contains a single stigma, supported by styles fused into a single column. Fruits are berrylike drupes ca. 69 mm in diameter containing 15 rugose, whitish seeds; ripe fruits have greenishblack or bluishblack (rarely yellow or white) skins and purple pulp (Fig. 1e). Ivy species have a wide range of chromosome numbers: H. helix

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is diploid (2n=48). Tetraploids and octoploids also occur in the genus Hedera. It is suggested

that the base number is x = 12 (Metcalfe 2005). This description of the plant is based on Tutin et

al. 1968, Lee and Richards 1991, Rose 1996, Larocque 1999, and Reichard 2000 as well as

personal observations by the authors.

(b) Distinguishing features – There are several Hedera species in North America that are

regarded as ornamental plants but escape into natural environments. Although most species of

ivy are commonly called ForEnglish ivy,Review more specifically, Only Hedera helix L., the most common

commercial and naturally occurring species is Hedera hibernica ‘hibernica’ (Kirchn.) Bean

(Murai 1999). There have been extensive debates regarding the taxonomic status of Hedera

hibernica var. ‘hibernica’ as a separate species or as a different variety of Hedera helix; there is

currently no general consensus on this issue (Sulgrove 1984; Metcalfe 2005). In an effort to

determine species along the west coast, the taxonomic identification of 58 populations of ivy

occurring throughout California, Oregon, and British Columbia was investigated in a study in the

1990s (Murai 1999; Clarke et al. 2006). Genetic analysis revealed that the majority of samples

taken corresponded to Hedera hibernica var. ‘hibernica’ (83%) and that only a small proportion

(13%) were comprised of Hedera helix L. The most invasive varieties of Hedera helix L. were

‘Baltica’, ‘Pittsburgh’, and ‘Star’. Another study sampled five locations on Vancouver Island

(Combers Beach, Wickaninnish Beach, Long Beach, Ucluelet, and Beck Island), and identified

all samples to be Hedera hibernica ‘Hibernica’. Variety ‘hibernica’ is distinguished by having

double chromosomes and larger, floppier leaves (Larocque 1999). Hedera species can also be

identified by the number and arrangement of rays on the hairs or trichomes (Beach 1981).

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Trichomes of H. hibernica lie parallel to the leaf surface and are 0.40.875 mm in size while

trichomes of H. hedera are erect, bristlier, and 0.751.062 mm in size (Ackerfield 2001).

Ivy is unusual in the forests of western Canada as there are very few largestemmed or

arborescent vines that occur naturally in this region (Larocque 1999). The native vine most

resembling ivy in British Columbia is Lonicera ciliosa (Pursh.) Poir. (Western Trumpet

Honeysuckle), identifiable by its deciduous, opposite leaves (Pojar and MacKinnon 1994).

McAllister and Rutherford (1990) suggest that cut twigs and petioles of H. hibernica is much

more powerful, distinctlyFor sweeter, andReview more resinous thanOnly H. helix.

cuttings has led to many different varieties, or cultivars, of Hedera spp. Many of these varieties

mutate back and forth from one to the other (Sulgrove 1987; Murai 1999). Currently, there are

over 400 cultivars of H. helix L., each having slightly different ecological tolerances. These

ecotypes are listed with the American Ivy Society (Headley et al. 1992). More than five percent

of sample ivies in North America had haplotypes similar to H. helix subsp. caucasigena (Green

et al. 2013). Other species, such as H. helix subsp. rhizomatifera, have recently been introduced

in the nursery trade and have not established natural populations (Green et al. 2013). Many

variations and related species to H. helix are adapted to warmer climates and may have difficulty

invading northern environments (Green et al. 2013).

3. Economic Importance

(a) Detrimental – In North America, especially near the coasts, ivy has become one of the most prominent invasive plants in forests located near urban areas or major roads (Fig. 2). Mishra et

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al. (1995) describes mechanisms by which vegetation such as ivy can cause building

deterioration by physical and chemical means. For example, expanding root and shoot tip

volume within walls can increase the size of cracks and fissures (Mishra et al. 1995). Chemical

deterioration includes the release of acidic compounds through roots may increase erosion on

stone buildings and foundation (Mishra et al. 1995; Mouga and Almeida 1997). Leybourne

Castle has become completely destroyed over a 100year period of time due to the growth of ivy

(Schaffer 2016). Although the damage that ivy causes to many tree species is detrimental, it is

not considered to be parasiticFor because Review it does not receive Only any nourishment from its host

(Okerman 2000).

The extent of damage caused to the host tree is commonly disputed among ecologists and

horticulturalists (Larocque 1999). Horticulturalists sometimes argue that ivy is not destructive to

trees and provides suitable habitat for forest fauna (Larocque 1999), whereas ecologists tend to

argue that ivy is detrimental to host trees, increases pathogen and disease through girdling, and

competes for light, water, and nutrients (Larocque 1999). Putz (1991) contends that lianas

(distinguished from “vines” on the basis of greater stem thickness and woodiness) compete with

the host trees for water, light and nutrients, and have the ability to deform and break tree stems,

increase accessibility to herbivorous animals, and decrease growth rates. It is also much more

expensive and damaging to harvest trees laden with lianas (Fox 1968; Appanah and Putz 1984;

Putz 1991). Shoup and Whitcomb (1981) examined interactions between host trees and ivy

ground cover and found that the ivy suppressed root development of cottonwood (Populus

deltoids Bartr. Ex Marsh.) by 32% and silver maple (Acer saccharinum L.) by 64%. Deciduous

forests such as the sensitive Garry oak (Quercus garryana Dougl.) ecosystems in southwestern

British Columbia and the adjacent states of Washington, Oregon, and California are particularly

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vulnerable to invasion by ivy because of its evergreen nature and ability to grow all winter while

native vegetation lays dormant (Thomas 1980). As ivy begins to shade out deciduous foliage, the

tree is suppressed and gaps are created in the canopy. Consequently, more sunlight reaches the

ivy promoting more rapid and voluminous growth of the vine itself (Thomas 1980). It is also

suggested that the additional weight of ivy, especially when covered in snow or ice, increases the

likelihood of tree damage during periods of high wind (Siccama et al. 1976).

Ivy forms thick mats of groundcover, also known as “ivy deserts” (Fig. 2e), where other plants seem to be unable Forto compete Review (Reichard 2000). TheseOnly “ivy deserts” block natural regeneration in forests and displace native species. A study examining the effects of ivy invasion on the vegetation in Stanley Park, Vancouver, B.C. showed a higher number of native plant species in sites with no ivy and a significant decrease in native species diversity with increased ivy density (Quinn and Best 2002). In invasive situations, it is often difficult to determine how many native plants the invader has directly displaced because of the complex indirect relationships and numerous variable impacts that exist in heavily invaded sites (Larocque 1999).

Native plants that are displaced at a site invaded by ivy are often species that have a close association with the native fauna (Reichard 2000). In Australia, “ivy deserts” have reduced feeding areas for wildlife such as lyrebirds and wombats. Lyrebirds are prevented from reaching the soil to obtain their food, and the grasses suppressed by the ivy are a key component of the wombat’s diet (Freshwater 1991).

Both the leaves and berries of ivies are mildly toxic and contain substances that can induce unpleasant symptoms or even death in certain concentrations (Rose 1996). Dermatitis and strong allergies can develop after prolonged exposure to Hedera spp. (Garcia et al. 1995;

Ozdemir et al. 2003). Three compounds have been isolated from H. helix that can cause irritation

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and sensitivity, even in low concentrations (0.03%) (Hausen et al. 1987). Only two of the

compounds (falcarinol and didehydrofalcarinol) are within the plant throughout the entire year

(Hausen et al. 1987). The allergen can sustain a great stability, invoking a dermatic response

after storage for six years (Garcia et al. 1995). Two case studies involving a 4yearold and 5

yearold resulted in itchy dermatitis, burning sensations, vesicular and erosive lesions, and

pigmentation (Massmanian et al. 1988). There have been cases where allergic reactions did not

develop until after months of handling the plant (J. Fraser pers. Comm.). Although a response is

not seen in every individual,For those withReview sensitive skin areOnly encouraged to wear protective clothing

while handling ivy (Ozdemir et al. 2003). The thick mats formed by ivy can serve as a refuge for

many unwanted rodents (Costello 1986). They can also serve as a reservoir for bacterial leaf

scorch (Xylella fastidiosa Wells et al. 1987), a harmful plant pathogen affecting many native

trees (Swearingen and Diedrich 2000).

(b) Beneficial – The ivy plant supports a multimilliondollar industry as a horticultural plant

due to its many desirable characteristics: it grows rapidly, it is inexpensive, it requires low

maintenance, and remains green all year (Murai 1999; Reichard 2000). For this reason, ivy is a

common garden and indoor ornamental. The American Ivy Society is an organization entirely

dedicated to the preservation of English ivy and its relatives through education and promotion

(The American Ivy Society 2002). Ivy has been incorporated into monumental architecture and

European décor, the motive for the Ivy League private schools in the United States. Ivy has been

widely planted for erosion control along roadways, embankments, and street medians. However,

it is actually ineffective in this role due to its shallow, matlike root system (Parker 1996; Ivy

Removal Project 2002). Lianas, such as English ivy and its relatives, play an active role in

nutrient cycling due to their rapid growth rates of voluminous leaf production (Schnitzler 1995).

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Litter produced in the spring leaches nutrients such as nitrogen that trees use during the growing

season (Trémolières et al. 1988). Trémolières et al. (1998) argues that cutting large lianas from

host trees to save them from being killed is misguided. Trees hosting large lianas produce larger

annual growth rings (Larocque 1999).

Cuce (2017) states that ivy produces the beneficial effect of regulating temperatures by keeping walls cool in the summer and dry in the winter. Internal wall temperature can be reduced by up to 6°C when a 10cm thick ivy wall is present during sunny sky conditions. Another study found that ivy greater thanFor 20 cm inReview thickness had an effectOnly on the temperature and increased humidity of the microclimate of vegetative walls; lowering the temperature when hot and insulating heat when cold (Sternberg et al. 2011). The transfer of heat is due to multiple variables

(conduction, convection, evapotranspiration) that lower or raise the temperature counter to the external environmental temperature (Cuce 2017; Grabowiecki et al. 2017). According to Rose

(1996), ivy does not damage walls or masonry but preserves them by protecting them from environmental elements. It is hypothesized that ivy has a “bioprotective” role on stone wall decay; alleviating rainfall intensity, direct solar radiation, freezethaw cycles, moisture evaporation, salt crystallization, and diminished light for microorganism growth (Sternberg et al.

2011). There is an ongoing debate on the advantageous and damaging effects of ivy growth on buildings.

Various parts of the ivy plant have been used for medicinal purposes over the past two

millennia to treat a variety of conditions ranging from headaches and ulcers to dysentery and the plague (Rose 1996). Hedera spp. are currently being considered as a potential cure for the

uncomfortable and sometimes fatal condition known as leishmaniasis (Ridoux et al. 2001;

Abbasifar et al. 2017). This condition occurs in tropical and subtropical regions throughout the

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world and is thought to affect over 400,000 people annually. Today, ivy is most often used as

homoeopathic treatment for a number of common conditions and diseases; extracts of the plant

are also being examined as possible ingredients in cosmetic creams and a tumour reducing agent

(Rose 1996). Studies have shown ivy extracts to be effective controls against liver flukes (Julien

et al. 1985), apple scab [Venturia inaequalis (Cooke) Winter] (Bossard 1992) and fire blight

(Erwinia amylovora) (Mosch et al. 1999). Leaves and stems are used to treat multiple ailments

and ivy is recorded in the European Pharmacopoeia as an herbal medicine due to the widely

accepted effectiveness byFor several EuropeanReview countries (SunOnly et al. 2016). Hederasaponin B extract

from H. helix can be used as a novel drug candidate with antiviral activity against subgenotypes

of enterovirus 71 (EV71), the foremost source of hand, foot, and mouth disease (HFMD) (Song

et al. 2014).

Beekeepers in Britain (Ivy Removal Project 2002) and in British Columbia have used ivy

as a winter source of pollen for their commercial bee hives (J.A. McDonald pers. Comm).

Moreover, ivy is described as a general toxin eliminator with superior removal efficiency (Yang

et al. 2009). In a study of the suitability of various plant species for improving indoor air quality

by NASA, it was determined that H. helix is able to remove formaldehyde, benzene, and

trichloroethylene from the air (Wolverton et al. 1989). Among 28 indoor plants, English ivy was

ranked as having the second highest volatile organic compounds (VOCs) removal efficiency

(Yang et al. 2009). When examining the removal of common VOCs, such as benzene, toluene,

octane, trichloroethylene, and ⍺pinene, H. helix was measured as having a removal efficiency of

38.33 ± 3.17 µg m3 m2 h1 over six hours during the day (Yang et al. 2009). English ivy thus

proves to be an excellent plant for indoor décor; easy to grow in lowlight conditions while

increasing air quality. Lastly, recent studies have examined stability and expression of reference

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genes in H. helix, promoting the use of reverse transcription quantitative realtime PCR in the

field of genetics (Sun et al. 2016).

Seeds Order, nor are they listed in British Columbia as a noxious weed under the Weed Control

Act. In 2002, English ivy was given noxious weed status in both Washington (class C) and

Oregon states (Washington State Noxious Control Board 2003; Oregon Department of

Agriculture 2003). EnglishFor ivy is listed Review in the Canadian Only Poisonous Plants Information System

(Government of Canada 2013).

4. Geographic Distribution

Hedera helix L. is a native of Europe, ranging from Ireland (sea level to 615 m) in the west, to

Latvia in the east at about 25º longitude; Hedera hibernica appears in a similar range at

approximately 10º longitude. Southern Sweden at 60º N latitude is the most northerly extension

of its range and the Greek island of Crete at 35º N latitude is the most southerly point (Rose

1996). The plant has been introduced to Australia, New Zealand, South Africa, Brazil, Hawaii,

and North America, where it is now considered naturalized. In Canada, ivy is found as a weed in

southwestern Ontario at Point Pelee National Park, and along the southern coast of British

Columbia (Fig. 3). On Vancouver Island, the plant has naturalized from Victoria to Port Renfrew

(Larocque 1999) and at least as far north as Port McNeil (B. McMullen pers. Comm). Ivy has

also been reported in Vancouver, the Gulf Islands and Call Inlet (B. Westgate pers. Comm.). In

the United States, it is found in at least 26 states including the District of Columbia (Swearingen

and Dreidrich 2000) with heavy infestations occurring along the west coast from central Oregon

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up to northern Washington and along the east coast from Virginia to New York (Reichard 2000).

Rehm et al. (2014) found that winter low temperature extremes are not a major limitation in the

center of its native range. With the anticipated intensification of global temperatures due to

climate change, it is expected that ivy may increase its invasion northward within Canada and

Europe, possibly triggering a more active invasive phase (Pitelka et al. 1997; Davis et al. 2005;

Walther et al. 2005; Clements and DiTommaso 2011).

5. Habitat For Review Only

(a) Climate requirements – The climate type is cool mesothermal for English ivy (Meidinger et

al. 2009). Hedera spp. are found along both the eastern and western seaboards of North America

in a variety of habitats ranging from moist, heavily shaded coniferous forests to dry, relatively

open deciduous woodlands (Larocque 1999). In British Columbia, the minimum, average, and

maximum elevation where ivy occurs is 18 m, 47 m, and 90 m (Klinkenberg 2013). The species

generally occurs near urban areas, from sea level to 1000 m elevation (Reichard 2000).

Individuals growing at higher, cooler latitudes are limited in terms of fruit production (Metcalfe

2005). Northernmost populations in Sweden and the northern regions of the former Soviet Union

are unable to sexually reproduce, relying on vegetative reproduction (Metcalfe 2005). Ivy is

limited by temperature (Thomas 1980). It remains in its juvenile form at its northern, eastern and

maximum altitudinal distribution limits even though juvenile parts are more often killed than

adult parts during severe frost spells. The ability of juvenile plants to regenerate from dormant

eyes ensures survival, while the loss of leaves impedes the change to the adult form

(Andergassen and Bauer 2002). For ivy to reproduce successfully, the mean temperature must

remain above 15ºC (Rose 1996) and for new internode growth to occur the temperature must

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remain above 10ºC (Rylko and Kacperaska 1981). However, heat stress can impair the photosynthetic process (Bauer 1978). The optimum temperature for growth of English ivy is

21ºC (Larsen and Mortensen 1987). The net photosynthetic rate does not begin to decline until temperatures reach between 3ºC and 4ºC, and even when temperatures drop to 8ºC, the rate is sustained to 8090% of the normal state (Bauer and Kofler 1987). Bauer and Kofler (1987) concluded that inhibition of the net photosynthetic rate of English ivy after severe frosts could be attributed to actual frost damage to the photosynthetic apparatus and not to the development of maximal frost tolerance. For Review Only

Investigations carried out by Murai (1999) corroborated the finding by previous studies that English ivy prefers direct sunlight, but endures a wide variety of light conditions including heavy shade. Hoflacher and Bauer (1982) determined that the ability to acclimatize to strong light is not fully developed in the juvenile phase; however, when grown in strong light, the juvenile form develops thicker leaves with a higher photosynthetic rate. Therefore, English ivy’s plasticity is largely due to the presence of two leaf types with different physiology characteristics suited for a specific level of light (Bauer and Thöni 1988; Larocque 1999).

(b) Substratum – English ivy thrives in a wide range of soils with a pH greater than 4 (Headley et al. 1992; Metcalfe 2005). Larocque (1999) noted that heavily invaded areas within selected sites throughout Greater Victoria were characterized as having at least several centimeters of dark brown, fine to medium textured soil. Moist fertile or very fertile soils (fairly dry to slightly damp) are favourable (Metcalfe 2005). In France, optimal plant growth was observed on calcareous, eutrophic and moist soils (Schnitzler, 1995). Although English ivy grows well in both basic and acidic soils (Reichard 2000), Willumsen (1986) reported the quickest rooting and

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subsequent growth of the plant when pH levels were between 4 and 6. Excessive amounts of

water could be a limiting factor for the growth of ivy (Reichard 2000). The minimum, average,

and maximum soil moisture regime (SMR) for ivy as recorded by Klinkenberg (2013) is is 3

(very xeric), 4 (mesic), and 7 (mesic). Salinity levels are best around 2.5dS m1 for H. helix, with

negative effects showing at 13dS m1 (Younis et al. 2014).

forest edges, fields, hedgerows,For flood Review plains, and generally Only any area where ground disturbance

has occurred (Swearingen and Diedrich 2000). Quinn and Best (2002) found that there is an

exponential decrease in ivy density with distance from roads and trails. On southern Vancouver

Island, the most heavily invaded sites examined by Larocque (1999) were located in Douglasfir

and Garry oak communities. It was also observed that the adult form of ivy was most

predominant within deciduous forests, whereas the juvenile form dominated within coniferous

forests. In B.C. plants in the shrub layer that are associated with ivy include exotics such as

Daphne (Daphne laureola L.), English holly (Ilex aquifolium L.), Himalayan blackberry (Rubus

discolor L.), and yellow archangel (Lamium galeobdolon L.), (J. Sargent pers. Comm; pers.

obs.). Native species associated with the shrub layer include sword fern (Polystichum munitum

(Kaulf.) C. Presl.), tall Oregon grape (Mahonia aquifolium (Pursh) Nutt.), dull Oregon grape

(Mahonia nervosa (Pursh) Nutt.), bracken fern (Pteridium aquilinum L. Kuhn), snowberry

(Symphoricarpos albus L.), trailing blackberry (Rubus ursinus Cham. & Schldl), baldhip rose

(Rosa gymnocarpa Nutt.), nootka rose (Rosa nutkana C. Presl), red elderberry (Sambucus

racemose L.), salmonberry (Rubus spectabilis Pursh), and more (pers. obs.). Ivy has been

observed to climb up trees such as Douglas fir (Pseudotsuga menziesii (Mirb.) Franco), western

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hemlock (Tsuga heterophylla (Raf.) Sarg.), and Pacific redcedar (Thuja plicata D. Don) (pers. obs.). Cities such as Surrey, BC, were found to contain more ivy than Himalayan blackberry when analyzing aerial data (Chance et al. 2016). However, Surrey parks contained more blackberry than ivy (Chance et al. 2016). Ivy may outcompete native species in BC for nutrients and decreases native species diversity with increased ivy density (Quinn and Best 2002). Ivy invasion has been assessed as negatively impacting the native community of species in British

Columbia (Quinn and Best 2002). Ivy is classified in the Modal nutrient regime class D and modal Biogeographic EcosystemFor ClassificationReview zone class Only CDF (Klinkenberg 2013). Differences in environment can shift the bacterial phyllosphere in ivy due to trafficgenerated particulate material. For example, urban environments in Belgium are dominated by the bacteria

Hymenobacter and Sphingomonadaceae, whereas nonurban environments contain Beijerinckia and Methylocystaceae (Smets et al. 2016). Inoculation of Pseudomonas sp. Stenotrophomonas sp. and Achromobacter increased water diffusing rates (water and mineral permeability) across isolated ivy cuticle by up to 50% (Schreiber et al. 2005).

6. History

Fossil records suggest that Hedera survived up to 5.8 million years ago (Metcalfe 2005).

However, chloroplast DNA data has shown that Hedera may have origins in the Tertiary period

(Ackerfield and Wen 2003). Diversification of Hedera is thought to have occurred in Europe,

Western Asia, and the Macaronesian region with allopolyploidization playing an impactful role in the speciation of Hedera (Ackerfield and Wen 2003). The unusual flowering periodicity aligns with the potential Tertiary period timeline (Ackerfield and Wen 2003). The earliest known association that humankind had with ivy was uncovered through pollen analysis and found in a

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settlement in Hampshire, England dating back to 5600 B.C.E. (Beach 1981). The first written

account of the species is from 314 B.C.E., when Theophrastus described the species in his

Historia Plantarum. English ivy was first imported to North America in 1727 near Wawa,

Pennsylvania and it quickly established itself as a popular ornamental plant among settlers (Rose

1996). Records of the species in British Columbia date back to 1892 when a Scottish

horticulturalist, George Fraser, introduced ivy to Ucleulet on Vancouver Island (Murai 1999).

The plant name gained recognition during the 1930s when the name of a group of eight

prestigious colleges alongFor the eastern Review seaboard was coined Only as “The Ivy League”, because ivy had

been planted along their buildings walls in an attempt to imitate European traditions (Rose

1996). Dozens of variations of ivy have been bred and sold throughout the horticultural trade

(The Ivy Society of America 2002).

Recently, the transformation of ivy from a highly regarded ornamental shrub to a

problematic invasive species has been occurring throughout a number of countries where its

ecological impacts are becoming known. Various organizations have formed worldwide to deal

with the problem including the Ivy Removal Project based in Portland, Oregon, which has

already removed over 100 ha of ivy from the heavily invaded Forest Park (Ivy Removal Project

2002). The spread of ivy has been tracked in urban cities and public parks, such as Stanley Park

in British Columbia (Bergeson 2009). It is estimated that out of the 250 ha of forested land in

Stanley Park in 2009, 12 ha were covered with ivy (Bergeson 2009). A recent study utilized

hyperspectral and LiDAR data to determine that 1.51 km2 within Surrey, BC was invaded with

ivy (Chance et al. 2016). Among these parks, ivy covered 0.35 km2 (Chance et al. 2016). Since

its introduction into North America, H. helix has grown rapidly in deciduous forests, forming

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large blanketed mats of vegetation (Okerman 2000). Despite the invasive nature, ivy continues to be sold in nurseries through North America and the world (Okerman 2000; Cronin et al. 2017).

7. Growth and Development

(a) Morphology – Ivy vines can grow to immense sizes if conditions are favorable, with some

reaching over 27 m in length and 30 cm in diameter. The weight of ivy removed from a single

tree in Olympic Park, Washington was estimated to be 953 kg (Simon 2002). Larocque (1999)

described differences betweenFor the heightReview attained by juvenile Only ivy and that of the adult plant; the

adult form averaged 11 m while the juvenile form averaged over 34 m. There was also a greater

average stem diameter for adult vines compared to juvenile vines and a positive correlation was

determined for both ivy height and diameter with respect to host tree circumference. Adult and juvenile leaves are referred to as sun and shade leaves respectively, though both morphologies

can occur in the sun; not in response to light or age but ontogenyrelated morphotypes (Rehm et

al. 2014). Leaf morphology often changes from juvenile to adult in conjunction with vertical

height, due to the whole shoot morphology growth in the canopy (Rehm et al. 2014). In its native

range, leaf phenotypes are expressed along the vertical profile; juvenile leaves crawling along the

forest floor while adult leaves are found in the canopy, with a transition zone midcanopy (Rehm

et al. 2014). This change from juvenile to adult leaves is referred to as phase change (Woo et al.

1994). The mRNA HW101, responsible for encoding a protein similar to lightharvesting

complex II, is more abundant in juvenile leaves (Woo et al. 1994). This increase in expression, in

addition to higher expression of one Lhcb gene, may correlate to the photosynthetic

characteristics seen between juvenile and adult leaves, relating to the phase change observed

(Woo et al. 1994). Rogler and Hackett (1975) successfully reversed mature leaves to the juvenile

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form using GA3; demonstrating that gibberellins, as a class of hormones, play a crucial

physiological role in maintaining leaf juvenility.

There is an increase in ploidy levels when examining the cells of callus in adult and

juvenile plants; this is thought to be a function of growth rate (BanksIzen and Polito 1980). The

trichomes in English ivy are short stalked with a central boss radiating multiple unicellular rays,

sometimes standing up at an angle to the leaf surface (McAllister and Rutherford 1990). One

isolated population in Sicily has been found to be a tetraploid but displays morphology like a

diploid H. helix (McAllisterFor and Rutherford Review 1990). Only

(b) Perennation – The evergreen habit of ivy allows it to photosynthesize throughout the entire

year (Reichard 2000). Cold weather may induce frost tolerance, allowing for survival of ivy in

temperatures as low as 25ºC (Metcalfe 2005).

demonstrated by Thomas (1980), who determined that in the shade (47% of full sunlight), the

leaf biomass was 2558 cm2 dm2 while in more open areas (6568% in full sunlight), the leaf

biomass increased considerably to 100 cm2 dm2. The maximum light absorbance of ivy is

between 400 and 700 nm (Metcalfe 2005). Some light is absorbed between 700 and 1350 nm,

with a slight reduction in absorbance around 550 nm (Metcalfe 2005). Therefore, ivy can persist

in irradiance of 3% full sunlight or less (Metcalfe 2005). Oberhuber and Bauer (1991) found that

winter stress induces nonradiative energydissipation in ivy, leading to photoinhibitory damage.

Leaf conductance has been found to be more sensitive to drought stress and more persistent in

the white portion of ivy leaves, whereas only blue light (light stress) had a direct effect to leaf

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conductance (Aphalo and Sánchez 1986). In comparison to other woody species, ivy was found

to contain the lowest chlorophyll content (Baldini et al. 1997). Ivy has been shown to contain

high plasticity despite the available light. Specific leaf area is 200 cm2 g1 in shade and 100 cm 2

g1 in sun (Metcalfe 2005). The lamina volume was found to be 1.4 cm3 (Sack et al. 2003).

During the growing season, ivy spreads very quickly, averaging 22 cm of new growth per month

(GOERT 2002) and as much as 1.4 cm per day for young shoots of H. hibernica (Rose 1996). As a vine, ivy has the advantage of focusing its available energy on rapid growth through elongation and leaf production, ratherFor than supporting Review stem tissues Only (Monsi and Murata 1970; Mooney and

Gartner 1991).

Rehm et al. (2014) found that photosynthetic capabilities were lower in adult leaves relative to juvenile leaves during end of winter and early spring, but reversed in midApril. It is hypothesized that this is due to frost resistance and inactivity. Additionally, vertical growth allows ivy to increase sunlight absorption by penetrating the forest canopy. Larocque (1999) found horizontal growth associated with ground creeping ivy was somewhat faster than the vertical growth up trees. A separate experiment revealed that ivy growing within 1.84 m of a tree will move towards it and then eventually grow upwards whereas any ivy growing beyond the

1.84 m will grow away from the tree (Ivy Removal Project 2002). The vertical growth up the tree will take place in juvenile form until the absence of abundant roots reduces the quantity of gibberellic acid in the plant and consequently causes a heteroblastic change to its adult form. An increase in gibberellin levels can cause a reversion from the adult form back to the juvenile form

(Lee and Richards 1991).

The nutrient levels of ivy leaf litter in France were: N = 0.08 g 100 g1, P = 0.031 g 100 g

1, K = 0.77 g 100 g1, Mg = 0.31 g 100 g1, C:N = 56.9% (Badre et al. 1998). Ivy attributes in

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understory of Galician woodlands were: 44.0 ± 7.4% actin depolymerizing factors, 16.6 ± 3.2%

lignin, 1.0 ± 0.6 silica, 63.4 ± 3.8% in vitro organic matter digestion, and 9.3 ± 1.2% crude

protein (GeonzálezHernández and SilvaPando 1999). The decomposition rate is between 30%

and 42% after sixteen weeks (Badre et al. 1998) but likely varies due to environmental

conditions. Water content based on fresh weight was found to be 65 ± 2% for both young and old

leaves from late summer to early spring (Parker 1962). Watersoluble protein in ivy leaves

gradually increase from summer to winter; possibly increasing sugar content and anthocyanins in

conjunction with cold hardinessFor (Parker Review 1962). Only

The climbing ability of ivy has long been of interest to scientists, with Charles Darwin

noting that aerial rootlets “secreted a little yellowish matter” to facilitate attachment to surfaces

(Darwin 1876). Functional aspects of this yellowish matter have only been worked out recently,

with Zhang et al. (2008) being the first to report that the adhesive force was due to nanoparticles.

The nanocomposite adhesive secreted by the ivy rootlets has an average force of 298 nN,

comparable to other reports of nanoparticlenanofiber adhesion (Xia et al. 2011). A limited

curing process of the adhesive allows it to fill gaps in the attaching surface; a combination of van

der Waals force and other forces (Xia et al. 2011).

(d) Phenology – Juvenile cuttings of English ivy undergo a heteroblastic shift to reproductive

maturity after approximately eight years of growth (Beach 1981). For mature plants, there is

great variability in the phenological patterns of the species. In a fouryear study by Snow and

Snow (1988), up to 34 month differences were seen in the flowering and fruiting periods of the

observed plants, depending upon the given location. In British Columbia, numerous bisexual

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flowers are produced in September through October. Fruits develop over the winter and ripen

during the spring, anywhere from March to May (J. Sargent, pers. Comm).

(e) Mycorrhiza – An unidentified specialized type of vesicular arbuscular mycorrhiza has been recorded on H. helix (Harley and Harley 1987). Hyphal linkages have been observed between H.

helix and grass (Newman et al. 1993). Eliminating floods has led to the development of

mycorrhizal fungi on ivy, increasing phosphorus uptake (Heuzé et al. 2009). There are no

reported studies on ivymycorrhizalFor Review associations within Only Canada.

8. Reproduction

(a) Floral biology – Hedera helix L. produces hermaphroditic white to yellowishgreen flowers

from late August until late November in umbels on the ends of fertile stems (Reichard 2000;

Metcalfe 2005). The first appearance of flowers under natural conditions occurs after 10 years of

growth (Clark 1983). Anthers are bright yellow to brownishyellow when falling off after

anthesis (13 days) (Metcalfe 2005). Smaller lateral inflorescences are also produced which

flower later in the season and either produce small fruit that abort the before ripening or fruit that

ripen laterally (Snow and Snow 1988). The upper portion of the flower’s ovary (above the

inferior ovary) contains the nectary consisting of secretory tissue, which is accessible to sugar

feeding insects (Ferrazzi 1988; Vezza et al. 2006). The nectary consists of parenchyma

containing chlorophyll covering xylem and phloem (Vezza et al. 2006). Nectar exudes from the

stomata, a green to brown colour during the flowering period, changing colour because of

anthocyanins in the subepidermal layers (midSeptember to early November) (Vezza et al.

2006). The flowers are most frequently pollinated by flies and, to a lesser extent, bees, wasps,

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and Lepidoptera (Rose 1996; Jacobs et al. 2009) belonging to Diptera (Syrphidae, Muscidae,

Tachinidae, Sarcophaidae, Caliphoridae) and Hymenoptera (Formicoidea, Vespoidea, Apoidea)

(Ferrazzi 1988). A study in Europe found that the most common pollinator were wasps, whilst

bees made infrequent visits (Jacobs et al. 2009). The introduction of a new bee species (Colletes

hederae (Schmidt and Westrich)) in England has changed the floral community for ivy with the

solitary bee species favouring ivy flowers as a pollen source (Jacobs et al. 2009). Although ivy

produces several billion pollen grains annually, it scarcely registers in the pollen assemblages of

an area due to its poor dispersalFor properties Review (Bottema 2001). Only Therefore, when Hedera is present in

deposited pollen assemblages at 1%, this indicates Hedera must be common in the forests of the

catchment area (Bottema 2001). Bottema (2001) estimated pollen production by a single H. helix

plant growing on a rooftop on two separate days in October as 1.27 X 109 and 2.03 X 109 pollen

grains (Bottema 2001).

(b) Seed production and dispersal – Larocque (1999) suggested that ivy is not dispersed over

long distances, as most seedlings observed were found in close proximity to the adult plants.

This is believed to be partially due to the large size and weight of the seeds, making it difficult

for the wind to transport them over great distances. In North America, the blackbird (Turdus

merula L.), European starling (Sturnus vulgaris L.), mistle thrushes, and American robin (Turdis

migratorius L.) have all been observed eating the berries of ivy (Murai 1999; Jacobs et al. 2009).

Bird species that feed on ivy berries have been categorized as agents for transversal dispersal

rather than longitudinal dispersal, with the vectors flying across the landscape instead of

remaining within the confines of a single forest (Kalkhoven and van Ruremonde 1991).

However, Barnea et al. (1993) speculated that the mild toxicity associated with ivy berries limits

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the number consumed in one foraging bout. This may have the effect of reducing the number of

seeds deposited in one specific location, consequently resulting in better seed dispersal. It was

also found that the toxicity decreased as the fruits matured, resulting in a greater number eaten

during the spring once ripening had occurred. Snow and Snow (1988) reported that, of all the

British wild fruits, English ivy seeds are among the most nutritious for birds. The seeds also

average only 89 mm in diameter, thus all but the smallest frugivorous birds easily consume

them. The role of mammals or rodents in seed dispersal is poorly understood, although it is believed that high populationsFor of foxes Review present in Australia Only promote the spread of English ivy in

forests (Freshwater 1991).

rates. Seeds are dispersed from November/December until as late as June (Metcalfe 2005). The

length of time required for germination depends on whether the pulp has been removed from the

seed; in one study, germination within intact fruits took approximately four weeks, versus eight

and a half weeks for seeds removed from pulp (Clergeu 1992). No significant difference existed between seeds that had the pulpremoved manually and those that were previously ingested by birds. This suggests that the only effect that birds have on seed germination is the facilitation of pulpremoval. Reichard (2000) contradicts this study by saying that seeds must be scarified before they can germinate. In its native range, seedling density was strongly positively correlated

with soil moisture (Metcalfe 2005). Seeds are able to germinate 614 days of planting and may be inhibited by light (Metcalfe 2005). There is no evidence for any extended period of seed

dormancy or a soil seed bank (Metcalfe 2005). Once germinating, the hypocotyl carries the seed

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coat on the cotyledons, shedding as it expands (Metcalfe 2005). Skototrophic (lightavoiding)

shoots develop, increasing the chances of encountering a structure to climb (Metcalfe 2005).

(d) Vegetative reproduction – Although ivy exhibits prolific seed production, vegetative

reproduction is chiefly responsible for its success as a species. Typical vegetative reproduction

manifests as a plant creeping along the ground via adventitious roots (Reichard 2000). The Ivy

Removal Project (2002) in Oregon strongly recommends the removal of all stems fragments

when pulling ivy out of theFor ground Reviewso that regeneration Only does not occur. It is also known that any

plant material remaining in contact with the soil has the ability to continue growth if enough

moisture is available.

Ivy in the juvenile phase can be easily grown from cuttings, whereas ivy in its mature

phase is much more difficult to propagate (Hess 1959; Geneve et al. 1991). For instance, Clark

and Campbell (1983) reported development of roots and shoots in 100% of the juvenile cuttings

after 3 months. In contrast, for mature cuttings there was an observed difference in growth

potential depending on whether the cuttings were grown with other mature cuttings (73%

growing after 6 months) or mixed together with juvenile cuttings (50% growing after 6 months).

Adventitious roots can form easily, and are more common in the presence of indole3 butyric

acid (Burris et al. 2012). Even in the presence of water, rootlets may form from a recently

detached stem of ivy. This makes ivy transplanting and vegetative propagation relatively simple.

9. Hybrids

Hedera helix readily hybridizes with other species of Hedera; The Ivy Removal Project (2002)

reported leaves of both H. helix and H. hibernica growing from the same vine. Identification of

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naturalized populations is complicated because of the mixture of ornamental and “wildtype”

genetics (Green et al. 2013). When testing for variations of Hedera in Washington, 77.4% of sampled plants were identified as the tetraploid H. hibernica (Green et al. 2013). Triploids, unknown to populations naturalized in Europe, Asia, and northern Africa, occurred within the northwest corner of St. Edward State Park in Washington, representing 3.5% of the sampled plants (Green et al. 2013). There was a significant difference in the patch size between cytotypes;

H. hedera was often small (18.3 m2 of ground cover) and H. hibernica was large (117.5 m2 of ground cover) (Green et al.For 2013). TheReview prevalence of H. Only hibernica may be the result of

ecological adaptation to contrasting climate conditions (Green et al. 2013). Increased frequency

of polyploidy is an adaptation observed in other invasive species [e.g. spotted knapweed

(Centaurea maculosa)] increased DNA content, cell size, and more robust growth (Green et al.

2013). Hedera helix (2n=96) crosses with the morphologically distinct Fatsia japonica (Thunb.)

Decne. &. Planch (2n=24) to produce Fatshedera lizei (Hort. Ex Cochet), with offspring

intermediate in characteristics of leaf surface morphology (Dehgan 1987; Marshall et al. 2017).

Despite the different ploidy levels and separate genera, hybridization still occurs through

crossfertilization (Marshall et al. 2017). Many hybrids between Hedera are thought to have

evolved through allopolyploidization (Vargas et al. 1999). Hedera helix ssp. helix is a diploid,

unlike the tetraploid H. helix ssp. hibernica, with no triploids observed (Metcalfe 2005).

Molecular analysis suggests that there is some genetic mixing in the native range and shifts in ploidy or hybridization are achievable (Metcalfe 2005). Using cpDNA, H. canariensis is thought to be the diploid maternal ancestor that hybridized with H. hibernica to form H. iberica

(Ackerfield and Wen 2003). The naturalized hybrid H. helix x H. hibernica was detected through

morphology and chromosome counts in 2005 within western North America and Hungary

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(Marshall et al. 2017). The diploid H. helix is dominant on the U.S. east coast, whereas the

triploid H. hibernica is dominant on the U.S. west coast (Green et al. 2013). Another hybrid

between H. helix and H. maroccana, both of which are diploids found within southern Spain, has

recently received the name H. × cazorlensis, (Marshall et al. 2017). Marshall et al. (2017)

identified and classified three new hybrids of Hedera with a morphological guide. As Hedera

species more frequently come into contact with each other, the occurrence of hybridization is

expected to increase (Marshall et al. 2017). Green et al. (2013) suggested that population studies

are required to understandFor the species Review phenotypic and geneticOnly variability.

10. Population Dynamics

Ivy has considerable longevity (Ewers et al. 1991); a 433yearold vine has been reported

(Schenk 1983). Two arborescent specimens of a variegated form are approximately 50 years old

at the Huntington Botanical Garden (Robbins 1957). During the first eight years, most of the

growth, depending on light availability, is in the juvenile form (Beach 1981); flowering occurs

two years later (Clark 1983). The relative growth rate of H. helix seedlings while watered every

12 days at field capacity was approximately 0.025 g g1 day1 (Sack and Grubb 2002). Once ivy

has established itself in an area, it can quickly become the dominant plant, outcompeting and

displacing native species. It exhibits a positive feedback mechanism by penetrating openings in

the canopy, increasing the amount of light absorption, which further promotes its own growth.

Harmer et al. (2001) showed that 60 years after abandonment of a farmland in Broadbalk and

Geescroft Wilderness, UK, English ivy had become the dominant plant in terms of ground

vegetation and proportion of trees climbed and covered. Areas in France that experienced

flooding were found to contain smaller and younger ivy populations due to anoxia (Schnitzler

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and Heuzé 2006). Decomposition rates in France were found to be more rapid in the spring than

in the summer (Badre et al. 1998). In North America, lianas are best adapted to high fragmented

and midtolatesuccessional forests (Teramura et al. 1991). Rapidly growing cities tend to be fragmented and located near forested areas that may harbor ivy. These areas are vulnerable to invasion by ivy, climbing onto host trees or forming ivy deserts (Chance et al. 2016; Personal obs. 2017).

11. Response to HerbicidesFor and OtherReview Chemicals Only

Ivy is tolerant of preemergence herbicides and the efficacy rates of different postemergence herbicides vary somewhat depending upon the given study, likely due to the waxy cuticle

(Okerman 2000). The effectiveness of herbicides depends on factors such as application rates, time of application, and stages of growth of the plant (Derr 1993). Glyphosate at 3.0 kg ha1 has been reported to completely control ivy when applied during the spring (Neal and Skroch 1985).

Mechanically wounding the plants has been shown to increase the effectiveness of herbicides.

Complete control of ivy was achieved with a 25% glyphosate formulation when used in

conjugation with a stringtrimmer (Costello 1986). Derr (1993) did not achieve complete control

with glyphosate but noted that single application of the herbicide (applied at 4.5 kg ha1) reduced

older shoot growth. When sprayed with a nonionic surfactant 2,4D at twice the rate of 1.1 kg

ha1 effectively controlled ivy (Derr 1993). Mechanical damage followed with 2,4D application

also provided control (Costello 1986). The highest percent control when applying glyphosate at

8.51 kg ae ha1 was found to be 89% (Yang et al. 2013). Treatment with 2,4D at 5.6 kg ae ha1 also resulted in 89% control of ivy (Yang et al. 2013). Combinations of both preemergence and postemergence herbicides did not increase effectiveness (Yang et al. 2013). Metsulfuron, at a

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rate up to 0.168 kg ha1 yr1, was found to be more effective than either glyphosate or 2,4D

(Yang et al. 2013). For application to the cut stems of climbing vines, the systemic herbicide

triclopyr is recommended (Ivy Removal Project 2002; Prasad et al. 2003). Higher rates of 1350 g

ha1 of tricopyr resulted in 85% defoliation of matforming H. helix vegetation in New Zealand

(James and Dowsett 2015). Cutting of ivy and application of triclopyr did not result in any re

sprouting in a study conducted in BC (Table 1) (Prasad 2005). (Scythe (pelargonic acid) is a non

selective herbicide that can destroy the leaf cuticle, allowing for the successfully application of

roundup (glyphosate), sinceFor glyphosate Review is not easily taken Only up in ivy (Okerman 2000). Therefore,

the combined use of pelargonic acid and glyphosate may be more lethal.

There have been a number of studies examining the effects of NaCl on ivy. It has been

reported that NaCl applied to the shoot severely damages the plant, whereas soilapplied NaCl

has little effect. Chlorine ion toxicity is thought to be responsible for the death of the plant and

not the sodium ion. The somotic effects associated with salt concentrations are also lethal

(Headley et al. 1992). Other methods such as the use of a controlled herbicidal droplet

application or electrostatic herbicide sprayer have been suggested as ways of avoiding the thick

waxy cuticle, which is nearly impervious to droplet application (Gilman 1999; Okerman 2000).

In the case of removing ivy upon monumental structures and stone, it may be advised to select

herbicides with minimal damaging effects on the structure directly. Mouga and Almeida (1997)

suggest that neutralization of acid herbicides using potassium hydroxide may reduce damage

caused to limestone through decreased dissociation of calcium carbonate without decreased

effect of herbicidal properties.

12. Responses to Other Human Manipulations

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A variety of effective manual and mechanical methods have been used for the control of ivy,

especially when habitat restoration (and not plant mortality) is the overall objective. The exact

method to be applied is dependent upon the given conditions at each individual site. Factors such

as terrain, density and depth of the mat, time of year, and physical extent of the infestation all

relate to which method should ultimately be used (Ivy Removal Project 2002). For a description

of the various methods, refer to the Ivy Removal Project’s website at www.noivyleague.com.

Reichard (2000) suggests that ivy growing along the forest floor should be cut and pulled,

making sure to remove allFor plant fragments Review so that vegetative Only growth does not resume. Vines that

have climbed upwards on trees or other vertical structures are also very important to eradicate because of their reproductive capabilities. Cutting the vines at the base of the tree effectively

kills the plant attached to the upper portions. During the manual removal of ivy in Sherbrooke

forest, Australia Freshwater (1991) estimated that one person effectively cleared a 10 m 2 area of

land every hour. In the seven months following this removal, he found that the number of native plants had increased from 15 to 21 species in the designated study plots. If soil disturbance becomes too great during ivy removal at a site, native species should be planted to facilitate their

introduction and reduce the invasion by the subsequent wave of exotic species (Humphries et al.

1991; Reichard 2000). Burning ivy plants and resprouts with a blowtorch has been used as a

control mechanism and resulted in some success (Reichard 2000). Home (1952) suggests

controlling ground ivy by spreading 1520 cm of hardwood sawdust over the infested area.

A study in Portland found that manual removal of ivy disturbs native plant life, but the negative effects are overcome after ten weeks of treatment; manual removal being an effective control method within a growing season (Stanley and Taylor 2015). A management plan for ivy in Stanley Park is described in Bergeson (2009). Management stages include a routine

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monitoring program utilizing volunteers to identify new and existing patches of ivy, a ranking

scale for infestation and vulnerability of a site, and minimize invasion through mowing, tilling,

and pulling (Bergeson 2009). Additionally, Bergeson (2009) states the importance of informing

the public and marketing the invasive characteristics that are commonly observed in Canada. The

Ivy Project, initiated in 2009, was an ivy removal group for Stanley Park, BC. Twelve scheduled

events occurred in 2011 along with hundreds of volunteers to repurpose invasive ivy into

structural art, successfully removing ivy without any regrowth in 2011 (The Ivy Project 2011).

Additional removal in 20122013,For involvingReview more than Only one thousand volunteers, successfully

eradicated ivy from 8,000 trees, shrubs, and stumps within Stanley Park, allowing for restorative

efforts to focus on other invasive species (Lus 2013).

The results of different ivy management treatments are summarized in Table 1 from

Prasad (2005). All treatments involved cutting ivy coupled with any additional treatment, such as

the application of triclopyr, a potential bioherbicide (Chondrostereum purpureum), and

mulching (Prasad 2005). The bioherbicide did not appear to be effective possibly due to the

phytoalexins and other mycelia inhibitory methods (Prasad 2005).

13. Responses to Herbivory, Disease, and Higher Plant Parasites

Herbivory

(a) Mammals – The mild toxicity associated with ivy is caused by glucoside, which is capable of

producing severe abdominal symptoms, excitement, difficult breathing and even coma in

humans. Adverse effects on livestock and other animals have been reported when a sufficient

quantity of ivy was consumed (Rose 1996). However, there are reported case of starving sheep

(Evans 1954) and goats (Martinez et al. 1985) surviving the winter snows by eating ivy. The

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European roe deer (Capreolus capreolus L. 1758) and European red deer (Cervus elaphus L.

1758) are known to forage on English ivy; the plant was found to be the fourth most digestible food item of six deer species studied in Europe (Oleffe et al. 1993). The fallow deer (Dama dama L. 1758) is also reported to graze on ivy near Pisa, Italy (Cassanova and Sonego 1988) and

European hare (Lepus europaeus Pall. 1778) will eat the plant as a last resort (Ivy Removal

Project 2002). In North America, however, there have been no reports of ivy herbivory. During

the course of clearing ivy from over 9000 trees and 100 hectares of land in Portland, Oregon, no

sample has ever been producedFor containing Review a bite mark (IvyOnly Removal Project 2002).

(b) Birds – Although ivy is toxic to most native songbirds, there are documented cases of

invasive bird species and other omnivorous, wideranging native bird species consuming its berries. These include the blackbird, European starling, American robin, English house sparrow

(Passer domesticus L. 1758), stellar jay (Cyanocitta stelleri JF Gmelin, 1788) and cedar waxwing (Bombycilla cedrorum Vieillot 1808) (Ivy Removal Project 2002). While Snow and

Snow (1988) found nine species of birds in Britain that fed on the pulp of ivy fruit, only the woodpigeon (Columba palumbus L. 1758) was found to actually consume the seeds.

(Ivy Removal Project 2002). A coccid (Lichtensia viburni Signoret) has been found on ivy in the

Netherlands (VanRossem et al. 1979) and a mite (Phytoptus hedericola Keifer) was found on the plant in Australia (KnihinickiDanuta and Boezek 2002). Metcalfe (2005) listed 16 beetles,

27 hemipterans, 27 lepidopterans, and a thrips as feeding on ivy in Britain.

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(d) Other non-vertebrates – Metcalf (2005) listed five species of mites that have been observed

feeding on ivy in Britain.

Diseases

(a) Fungi – Biological control measures have rarely been attempted with ivy and it is unlikely

that such measures would ever be implemented as an eradication tool. This is because the

horticultural community uses Hedera species widely as an ornamental landscape plant. In Italy, a

severe disease of ivy causedFor by the Review fungus Phoma hedericola Only (Durieu & Montagne) has been

reported (Ciccarese et al. 1992). Also in Italy, some populations of ivy have been completely

desiccated, with the causal agent determined as the fungus Fusarium solani (Mar.) Sacc.

(D’Aulerio and Marchetti 1996). Some Phytophthora species such as P. palmivora (Butl.) Butl.

(Uchida and Aragki 1978; Ann 1993) and P. cinnamomi Rands (Pc) (Thinggaard and Toppe

1997) are reported to have caused root rot, stem, and leaf blight of ivy. Colletotrichum trichellum

(Fr.) Duke has caused anthracnose in ivy within Korea (Kim et al. 2001). Zeller (2014) was able

to stimulate a resistance towards fire blight in ivy, accelerating the defense response. Other

diseases of ivy include a leaf spot disease caused by Phyllostictina hederae, (Bose et al. 1970)

Xanthomonas hederae (Arn.) Dowson (McCain 1976), and powdery mildew caused by Oidium

araliacearum (Saenz and Koike 1998). The fungus Diaporthe eres has been found to infect

Hedera helix leaves, producing two main phytotoxins, 8hydroxy3,5dimethylisocoumarin and

tyrosol (Meepagala et al. 2017).

(b) Bacteria – The proteobacteria Xanthomonas hortorum pv. hederae can cause bacterial leaf

spot disease on ivy; 510 mm diameter spots on leaves surrounded by a chlorotic green halo with

greenishbrown watersoaked margins encircling the center, enlarging (Trantas et al. 2016).

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(c) Viruses – Rhabdovirus particles (6070 mm; varied length found) within the cytoplasm of ivy is known to cause ivy vein clearing virus (Miličić and Plavšić 1985). Arabis mosaic virus (AMV) can affect H. helix seedlings and cause foliage diseases (chloroticyellow vein banding) (Cooper

1993).

Higher plant parasites

Ivy can be parasitized by ivy broomrape, Orobanchae hederae Duby, but no apparent adverse effects were reported on the host plant (Sareedenchai and Zidorn 2008). One account of Indian dodder, (Cuscuta refleca ForRoxb.), growing Review on a greenhouse Only plant in Dublin, Ireland has been reported (Rose 1996).

Acknowledgements

This work was supported with funds from the Interdepartmental Recovery Fund, Canadian

Forest Service, Trinity Western University, and Natural Sciences and Engineering Research

Council of Canada. The authors thank Arthur Robinson and Barbara Hendell (Pacific Forestry

Centre) for advice and discussions, Adrienne McDonald (PFC), Delia Anderson (Trinity Western

University), and Eric McDonald for illustrations, Satish Bundel for technical help, and Bill

McMullan (British Columbia Ministry of Forests), Steve Rogers (British Columbia Ministry),

Jamie Kantor (International Forest Products Ltd.), Brian Westgate (International Forest Products

Ltd.), Scott Muir (Western Forest Products Ltd.), Michael Oldham (Ontario Natural Heritage

Information Centre) and Jim Heppner for information on ivy distribution in British Columbia and Ontario. We are grateful to Simon Shamoun, Richard Winder, and Art Robinson, as well as

Darren Robinson and an anonymous reviewer for providing reviews of previous versions of the manuscript. We thank the following herbaria for making material available for study: UBC, V,

https://mc.manuscriptcentral.com/cjps-pubs Page 35 of 56 Canadian Journal of Plant Science

DAO, PNW, and TRT. We gratefully acknowledge permission to reproduce the table from

Prasad (2005) from Research Information Inc.

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Table and Figure Legends

Table 1. Influence of various treatments on resprouting of English ivy (Hedera helix) in British

Columbia after 2 years (from Prasad 2005, reproduced here with permission). The experiments were laid out in a randomized block layout, and installed at three different sites to minimize variation of edaphic factors, with 10 replicates at each of the three sites. Observations on resprouting behaviour (number, height and vigour) were recorded for 2 consecutive years.

For Review Only

Fig. 1. Drawings of the ivy species complex found in British Columbia [Hedera helix L. and

Hedera hibernica (G. Kirchn.] Bean. A. juvenile leaf; B. adult leaf; C. single flower; D. flower cluster; E. fruit cluster (Drawings by D. Anderson)

Fig 2. Photographs of the ivy species complex found in British Columbia [Hedera helix L. and

Hedera hibernica (G. Kirchn.) Bean]. A. typical juvenile leaves; B. adult leaves and flowering stems; C. flower cluster; D. vines climbing trees in North Vancouver, British Columbia; E. “ivy barren” in North Vancouver, British Columbia.

Fig 3. Distribution of invasive Hedera ivy species [Hedera helix L. and Hedera hibernica (G.

Kirchn.) Bean] in Eastern and Western Canada based on herbarium collections from the UBC, V,

DAO, PNW, and TRT herbaria as well as eflora BC. See Holmgren et al. (1990) for institutional abbreviations.

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Table 1. Influence of various treatments on re-sprouting of English ivy (Hedera helix) in British

Columbia after 2 years (from Prasad 2005, reproduced here with permission). The experiments

were laid out in a randomized block layout, and installed at three different sites to minimize

variation of edaphic factors, with 10 replicates at each of the three sites. Observations on

resprouting behaviour (number, height and vigour) were recorded for 2 consecutive years.

______Treatment For Review Only Re-sprouting (%) ______Cutting alone 98.0 Cutting and triclopyr herbicide 0.0 Cutting and Chondrostereum purpureum bioherbicide 95.0 Cutting and black plastic mulch 0.0 ______

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Fig. 1

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Fig. 3

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