The Academic Review: How box blight of Buxus spp. is changing the landscape in the 21st Century.

IntroductionBuxus spp is an important plant in history as well as in today’s world. The first formal clipped box

was used by the Egyptians in 4,000BC (Topiary Arts, 2016). Throughout history and still today box is

used as the structural, formal element in gardens and landscape design. It has been used as a means

of execution of ‘control of nature’ and as a status symbol of wealth and also for medicinal purposes

(Topiary Arts, 2016). However this iconic plant species is under threat in the wild as well as in man-

made landscapes and gardens. The pest and diseases that affect the Buxus spp. are many. However

in this paper the main focus will be Box Blight’s impact on landscapes and horticulture.

Historic importance of the Buxus spp. in the UK.In the UK particularly the native Buxus spp was growing wild until the Ice Age whereupon the native

spp. was destroyed. However the Roman invasion in 100BC re-introduced the species (Topiary Arts,

2016). In the Middle Ages and through to the Elizabethan period the Buxus was used for knot

gardens, hedges, galleries as well as individual specimen displays after it was found that cypress spp

were not as reliable (Topiary Arts, 2016). The Hampton court gardens of Henry VIII had box spheres,

cones and animals (Topiary Arts, 2016). Topiary was born as a status symbol and to indicate control

of nature. Through the 17th into 18th century the naturalistic movement led by Capability Brown saw

Buxus’ usage decline as it was no longer fashionable to impose formality onto the landscape (Wilson,

2014). In the 19th century the return of formality came in a re-birth of the ‘Italian Renaissance’ The

Buxus became a staple; carpet bedding schemes, low hedges and extreme topiary designs of crowns,

birds dominated landscape design and parks. Nurseries in the UK were becoming specialised in

topiary works and selling ‘already formed’ plants in containers to the public (Topiary Arts, 2016). The

return of ‘knot style’ gardens and parterres became the identity of the ‘British Garden’

In the 20th century the Arts and Craft movement meant that the harsh control of nature was relaxed

though informal border designs with planting schemes and layout did not banish the box but

incorporated it as a backdrop and structural element within a design. Topiary was less extreme in

design. In the 60’s the public went through the ‘Front Garden Movement’ with classic rose beds and

the use of topiary and hedging was popular. We still see the Buxus as a stable plant in the garden

and in structural landscape designs and use it heavily for creation of shapes and backdrops. In the

urban landscape it is used in low line front hedging as a protective and framing barrier around

planting schemes and the topiary ball and pyramid is used outside establishments such as hotels,

restaurants, shopping centres and public houses to mark formalised entrances to buildings.

The Main threats to Buxus spp. The Box Caterpillar Moth – Cydalima perspectalis has become an increasing threat in recent

years. The Box Caterpillar entered Europe in 2007 and in 2011 the pest had fully reproduced in this

country. In 2012 this caterpillar replaced the molluscs spp. (snail/slug) as the most troublesome pest

in a poll conducted by the RHS (Appleby,M. 2013). By 2014, it had become fully established in

London and the home-counties (Royal Horticultural Society, 2016). These caterpillars cause

defoliation by eating the foliage (Plate 1) and in clipped Buxus cause full dying back of the plant in

high density feeding areas. The caterpillar protect themselves with white webbing during feeding

and pupation.

Plate 1 - The Box Tree Caterpillar Image Source; Royal Horticultural Society https://www.rhs.org.uk/advice/profile?pid=760

Caption: Identification information; The moth eggs are laid on the underside of the leaves in an overlapping/flat sheet formation and have a greenish/yellow appearance. The young caterpillars have yellow/green bodies with a black head, as they mature the body has black and white striping down the sides. The adult moth have white wings with a brown rim border.

There is chemical treatment available for the caterpillar as well as a pheromone treatment for

attracting the adult staged moth into traps (Royal Horticultural Society, 2016). The impact of this

invader on the UK is a cause for concern as it has the potential to attack our wild box trees and have

a large impact on our hedges, topiary specimens.

Box Blight - There are two genetic strains of the fungal disease; Cylindrocladium buxicola (now

known as Calonectria pseudonauiculata) affecting the whole Buxaceae family. The second;

Pseudonetria buxi only affecting the Buxus spp (Royal Horticultural Society , 2015; Ivors, 2016;

Horticulture Week, 2015). The fungal infections co-exist with one another most often on a plant

Cylindrocladium buxicola being the most serious of the two (Royal Horticultural Society, 2015; Ivors,

2016). Both strains exhibit the, browning and spotting on leaves, and defoliation, dying back patches

(Plate 2) which leads to death of the plant (Henricot & Wedgwood, 2013; Royal Horticultural

Society , 2015; Horticulture Week, 2015). The Cylindrocladium buxicola affects stem tissues in

addition with black streaks and die back (Henricot & Wedgwood, 2013) The spores of the fungi are

distinctly different and in wet weather can be seen. The Cylindrocladium buxicola has white spores

and the Pseudonectria buxi has pink spores (Royal Horticultural Society , 2015; Ivors, 2016).

Plate 2 - Box Blight Image Source; Royal Horticultural Society https :// www.rhs.org.uk/advice/profile?pid=96 Caption: A Fungal disease affecting foliage and is spread by moisture and overwintering reproductive soil borne spores. Classic symptoms of browning and sudden dying back and death spots can take hold very quickly.

Climate ChangeAs we know climate change globally is affecting many organisms and plant life. From the statistics

and analysis of the UK’ s climate change forecast (UKCP09) report it projects that warmer and wetter

winters and drier but more humid summers will become the UK climate (UK Climate Projections -

Met Office, 2009). This will result in a rapid increase of fungal infections and speed of spread of box

blight and other fungal infections in the UK (Forestry Comission, 2015). The wetter soil conditions

will also increase the risk of root rot diseases for the Buxus and of course other plants.

The Significance of Box Blight affecting Horticulture. It is a world wide spread problem. (Plate 3) There are 70 species of Buxus worldwide which are

mainly in the tropical and subtropical regions, 30 reside in Cuba and 17 are native to Madagascar

(Wilson, 2014). The rest of the Buxus spp are spread across the Caribbean, China and the Americas

including Latin America (Henricot & Wedgwood, 2013; Wilson, 2014). The Native European and

Asian Buxus are the only frost hardy species. The true origin of the disease is unknown. The earliest

record of the disease was found in the UK in 1990’s (Henricot & Wedgwood, 2013; Ivors, 2016;

Wilson, 2014; Weeda, S. M et al, 2012; Horticulture Week, 2015) in a Hampshire nursery (Appleby,

M. 2013). From 2002 onwards it had spread through Europe and to New Zealand (Weeda, S. M et al,

2012). In recent years it has spread to the Americas and East Asia (Henricot & Wedgwood, 2013;

Ivors, 2016; Wilson, 2014, Weeds, S.M et al, 2012).

Plate 3 - Worldwide Map of Box Blight infections. Source; Authors own creation with map image from http//:mapsofthe world.com.

The Native Buxus semperviens located in Surrey was reported in 2000 to have Box Blight present

(Appleby, M. 2013) and the Turkish native collection confirmed infection in 2011 (Lehtrijarvi, 2014)

which is of great concern.

Production and Commercially Commercially the sales of the Buxus have dropped in recent years due to the fear and stigma

attached to the plant. In addition some nurseries are unknowingly selling infected plants to the

garden centre sector by not fully understanding the diseases identifiable markers. However in some

cases there has been poor practice by nurseries and producers by suppressing infected plants with

fungicides ready for sale and the garden centres suddenly experiencing explosions of box blight from

the re-emergence (Henricot, B. 2013; The European Boxwood and Topiary Society, 2014). Nurseries

such as Buckingham Nurseries diversified due to seeing Buxus sales drop by 50% and the sales of the

alternatives increasing (Appleby, M. 2013). However some of the alternatives are currently in short

supply as many establishments have not fully/speedily diversified. Some of these ‘replacement of

box plants’ are vulnerable in themselves as such as Lonicera spp. because they tend to be mass/over

produced and this in turn could further cause weaknesses to other diseases (Appleby, M. 2013).

Historic/Visitor Attraction Gardens and Landscapes In the amenity sector of horticulture Box Blight greatly affects the finances of visitor attractions as

well as the aesthetic appearance and historic, iconic character of a landscape (Reid, 2015; Watkins &

Wright, 2007; Wilson, 2014; The European Boxwood and Topiary Society, 2014). The economic

damage that the infection can inflict upon an establishment can run into the thousands. The fact

that Buxus is slow growing; and it takes 18 years to grow and shape a large topiary ball means that

specimen would be worth £1,000 if not more (Wilson, 2014). When an infection breaks out the need

for pathology reports, closure of the site during infections, the fungicides, and man power in itself

and the operation of removal of infected material and replacement planting are all factors arising

from Box Blight infection (Reid, 2015). In many historic landscapes the Buxus is the most important

structural plant and the loss/damage the disease causes more than financial and practical problems.

In some establishments the spread of it can be so horrific and fast (48hrs) (Reid, 2015; Horticulture

Week, 2015) the devastation and loss of key and special specimens can hit hard. Ickworth Park the

Italianate Renaissance Gardens were repeatedly struck over a ten year period and a massive

infection in 2015 wiped out 80% of the hedging including a specimen that was over 200years old

(Reid, 2015). Up and down the UK managers of landscapes, gardens and visitor attractions are having

to make difficult decisions in regards to how best to manage the disease and the future of the design

and plant selection for these establishments. The combination of cultural practices and hygiene

management with fungicides is only working upto a point.

Management of the Disease and New Developments – Is there a way forward?Buxus spp Genetics The study of susceptibility to the box blight disease has been extensively researched and it has been

found that there are some species and cultivars that appear to be more resistant to the infection

(Shishkoff, 2015) but this is debatable as the studies show that the resistance is not a ‘complete’

resistance. Eventually they do all succumb to the box blight infection and that resistance is marginal

(Yonghong, 2015). Even though the genetic variation of the genus is wide it has proven difficult to

breed Buxus (Laere & Hermans, 2015). However there is currently some optimism in terms of

breeding. The scientific community is increasing further understanding of the characteristics of the

Buxaceae family. The leaf structure of a particular spp. such as thicker leaf cuticle/epidermal tissue

layers and a smaller leaf surface area indicate a physiological design that proves to provide ‘a level’

of plant defence from the fungus (Shishkoff, 2015). This is particularly apparent in the macrophylla

sub species of Buxus having a higher tolerance and lower susceptibility compared to sempervirens

but the variety of cultivars had a significant genetic impact of the resistance level within these sub

species groups (Henricot & Wedgwood, 2013; Shishkoff, 2015; Yonghong, 2015). However the

techniques of testing susceptibility need more refining as field trials and laboratory scenarios are

very different and using inoculated cuttings is very different to using plant specimens (Henricot,

2013; Yonghong, 2015).

A new development of a SSR-cDNa library has been created to look for particular genetic markers.

845 of these have been isolated from mRNA material and from those 23 polymorphic primer pairs

have been identified (Thammina, 2014) as key genetic charatisitic that can be used for Box Blight

resistance in genetic diversity, hybridisation and cultivar breeding of Buxus (Thammina, 2014).

Hybridization of Buxus to F1 from cross combinations resulting in 4750 ‘interspecific’ F1 seedlings

has recently been achieved in 2015 with a seed germination rate between 0-47%. (Laere & Hermans,

2015). However these are early days and the interspecific range of those seedlings may/may not be

variable or successful but the hybrids could offer the scientific community the opportunity to exploit

the F1 for desirable traits (Laere & Hermans, 2015).

Biological Understanding of the Funguses Life CyclesIn a taxonomic re assessment of Cylindrocladium buxicola (reclassified as Calonectria pseudonavicala

now) the fungus has two genetic clades unearthing a new phylogenetic species ‘Calonectria

henricotiae’ (Gehesquière, 2016) as an additional variant of the Box Blight disease which has a

greater tolerance to higher temperatures and increased tolerance to fungicides (Gehesquière, 2016).

This new information is worrying but the community know that there is more variance in the fungal

family now and more research can be undertaken (Gehesquière, 2016). The two strains of Box Blight

have very different overwintering mechanisms. It was found that the Cylindrocladium buxicola has a

unique overwintering structure form; ‘Microsclerotia’ which allows the fungus to reproduce during

winter months within soil. This explains how repeated re infection occur from leaf litter material and

dirty tools/machinery as this cell structure can survive for 5years within leaf material and upto 15

years in soil and in minus figure temperatures (Weeda, S. M et al 2012; Ganci, 2013). This

evolutionary adaptation in the Cylindrocladium buxicola is not present in the Pseudonectria buxi

strain of the fungus (Weeda, S. M et al 2012) which confirms how and why one strain is more

rampant and more difficult to treat in comparison to the other strain. This could unlock what types

of fungicide to use and tailor make compound ingredients to target this aspect of the funguses life

cycle in the future.

Fungicides The EU have recently banned some fungicides that are used in the treatment of the disease (Royal

Horticultural Society , 2015). The EU regularly reviews chemical substances and this means that

horticulturists across the industry have to keep upto date with the use of fungicides and other

chemical treatments (Royal Horticultural Society , 2015; Wilson, 2014). There have been a few

studies into the effectiveness of them against Box Blight but mostly so the Cylindrocladium buxicola

strain. They have been inconclusive or offer a suppressive/moderate level of control. However a

recent study evaluated and tested various products and found that one all-round product

‘Opponent’ completely eradiated box blight and timing and choice of fungicides such as ‘Bravo’,

‘Octave’ and ‘Signum’ greatly affected how well those products worked (Henricot & Wedgwood,

2013). However these are all commercial products that the public cannot access. The study did

however find that ‘Fungus Clear’ which is on the public market, did offer a moderate control but still

this does not really offer a total solution to the general public.

Plant Selections The Buxus spp as discussed has limited resistance to the disease but the following table show more

tolerant species which could still be used within a landscape or sold commercially to customers

whom still desire box plants. (Table 1) There are a wide range of alternative that can be used instead

of Buxus if the decision is to be taken to avoid all Buxus spp (Table 1) but this not the solution and

other alternative have their own pitfalls.

Table 1 - Collective list of Buxus spp to avoid and use and alternative plant selections. Authors own consolidation from a range of sources.

Buxus spp to avoid using More tolerant Buxus spp Alternatives to Buxus

B. sempervirens B. microphylla ‘Compacta’ Euonymus fortunei (various)B. sempervirens ‘Elegantissima’ B. sinica var. insularis ‘Winter Beauty’ Rosmarinus officinalis B. sempervirens ‘Suffruticosa’ B. sinica var. insularis ‘Pincushion’ Lavandula angustifolia B. sempervirens ‘American’ B. microphylla ‘Faulker’ Ligustrum OvalifoliumB. sinica var insularis ‘Justin Brouwers’

B. macrophylla ‘Trompenburg’ Ilex crenata

B. sempervirens ‘Marginata’ B. harlandii Lonicera nitida and Lonicera nitida ’Baggins Gold’

B. sempervirens ‘Jensen’ B. microphylla ‘Golden Dream’ Podocarpus lawrencei, salignus and andina

B. sempervirens ‘Pendula’ B. microphylla ‘Winter Gem’ Taxus baccataB. sempervirens ‘Scupi’ Myrtus communis

Berberis various

Hebe ‘buxifolia’ and ‘odora’ (short term solution for urban building enterances)

Good Practice and Strategic Methodology Non-chemical/ good practices are important to prevent a wider spread of box blight from outbreaks

however they are limited with dealing with infections alone. The combination of fungicide treatment

and good practice offer a moderate control of the disease (Royal Horticultural Society , 2015). It has

been know that some Buxus do survive after an infection but have a high risk of infecting other

surrounding specimens and are likely to become re-infected again.

Below is a range of advisory information that considers chemical and non-chemical options.

The current advice for dealing with box blight infections without fungicides emphasises good

hygiene practice with machinery, pruning equipment and PPE/clothing by using disinfectant

and washing clothing articles regularly (Horticulture Week, 2015; Ganci, 2013; Ivors, 2016;

The European Boxwood and Topiary Society, 2014; Royal Horticultural Society , 2015).

When an infection is identified it is important to ascertain which or if co-existence of strains

are present (Reid, 2015; Henricot & Wedgwood, 2013; Ivors, 2016). That way the decision

whether to use fungicides and practice operations such as pruning out material can be

examined (Royal Horticultural Society , 2015). The removal of all dead, dying and infected

material should be incinerated and soil disposed of in accordance to legislation (Reid, 2015;

The European Boxwood and Topiary Society, 2014; Horticulture Week, 2015; Watkins &

Wright, 2007).

Overhead irrigation increases the spreading potential of the fungus so this should be

avoided (The European Boxwood and Topiary Society, 2014). Drip irrigation in the

commercial setting offers a reduction in risk (Wilson, 2014).

Reducing the clipping regime of hedges and topiary should be considered where possible as

tightly clipped specimens have poor air ventilation and this increases the risk of infection

(Royal Horticultural Society , 2015; The European Boxwood and Topiary Society, 2014).

Landscape and Commercial Managers should take cuttings from non-infected material and

build a ‘safety bank’ of specimens (The European Boxwood and Topiary Society, 2014) so if

infection strikes the replantation costs are reduced by the creation of your own stock.

Application of mulch on soil areas could assist in reducing re-infection from fungus spores

left in the soil (CU Cooperative Extension Team, 2015).

Conclusion Commercial growers, nurseries and landscape managers need to select, evaluate and plan how they

wish to use fungicide products on the basis of their situation or preventative methods of protecting

their box plants. The scientific community are discovering more and more about the disease and the

Buxaceae family in which genetic screening, cataloguing and breeding programmes are beginning to

develop methods of producing plants with traits that could prove significant in disease resistance

and increasing tolerance levels. The morphological understanding of the fungus has shed light on a

new sub strain of the disease from Cylindrocladium buxicola and led a nomaculture reclassification

of that strain to Calonectria pseudonviculata. The fungi life cycle and reproductive mechanisms have

been explored and this in turn may offer a soil treatment in the future. The assessment and attitude

to the usage of Buxus species in the landscape is that even with the disease being present there are

ways forward in terms of alternatives and different selections of box plants. Still there are fears of

Native spp. areas will be greatly affected by the disease, climate change and other pest and disease

infections. The combination of hygiene and fungicide treatment offer a slow down to the spread of

the disease but do not offer a true eradication. Fungicide development in correlation to

understanding the disease will eventually become a significant method to possibly eradicate it.

Currently fungicide offer suppression and containment but the development of new products are

proving to be increasingly effective and the timing of applications have proven to be a breakthrough

in the management of the disease. Only time, science and effective management will determine how

far this disease takes hold and the outcome for the Buxus spp as a plant.

Word Count 2,804

References Appleby, M. (2013) ‘Box blight disease continues to strike box hedges’ The Telegraph Online Article written 11th February 2013 Telegraph Media Group Limited 2016 http://www.telegraph.co.uk/gardening/plants/9862995/Box-blight-disease-continues-to-strike-box-hedges.html [Accessed 14th February 2016]

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Gehesquière, B. et al, 2016. Characterization and taxonomic reassessment of the box blight pathogen Calonectria pseudonaviculata, introducing Calonectria henricotiae sp. nov. Plant Pathology, Volume 65, Issue 1, pp. 37-52.

Henricot, B. & Wedgwood, E., 2013. Evaluation of Foliar Fungicide Sprays for the Control of Boxwood Blight, Caused by the Fungus Cylindrocladium buxicola. Plant Management Network - Plant Health Progress , http://www.plantmanagementnetwork.org/pub/php/research/2013/boxwood/ [Accessed 14th Feburary 2016]

Horticulture Week, 2015. Pest and Disease Management - Box Blight. [Accessed 14th Feburary 2016].

Ivors, K., 2016. The North Carolina State University - Box Blight Guide. https://yancey.ces.ncsu.edu/wp-content/uploads/2013/02/Boxwood-Blight-Guide-01.03.13.pdf?fwd=no[Accessed 14th February 2016].

Laere, K. V. & Hermans, D. e. a., 2015. Interspecific hybridisation with Buxus spp. Scientia Horticulturea, Volume 185, pp. 139-144.

Lehtrijarvi, A., 2014. Cylindrocladium buxicola is threatening the native Buxus sempervirens populations in Turkey. Plant Protection Science, Volume 50, Issue 4, pp. 227-229.

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Thammina, C. et al, 2014. Development of polymorphic genic-SSR markers by cDNA library sequencing in boxwood, Buxus spp.. Applications in Plant Sciences, Volume 9, Issue 12.

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List of PlatesPlate 1 - The Box Tree Caterpillar Image Source; Royal Horticultural Society https://www.rhs.org.uk/advice/profile?pid=760Plate 2 - Box Blight Image Source; Royal Horticultural Society https://www.rhs.org.uk/advice/profile?pid=96Plate 3 - Worldwide Map of Box Blight infections. Source; Authors own creation with map image from http://mapsoftheworld.com

List of TablesTable 1 - Collective list of Buxus spp to avoid and use and alternative plant selections. Authors own consolidation from a range of sources.