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Home , Apiognomonia veneta, Campylomma, Corythucha, Corythucha arcuata, Corythucha ciliata, Corythucha cydoniae

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Task 5.6. Control of arcuata

Evaluating the Control and Management Options for Lace Bug ()

Rachel Down and Neil Audsley (Fera)

31st March 2019

Work Package 5 Control

Table of Contents

Abstract …………………………………………………………………………………………………………………………………………..2

Chapter 1. Introduction …………………………………………………………………………………………………………………..3

Chapter 2. Control options ………………………………………………………………………………………………………………9

Chapter 3. Oak lace bug in …………………………………………………………………………………………………29

Chapter 4. Uncertainties identified in the literature that would benefit from further research ……..36

Conclusions …………………………………………………………………………………………………………………………………...37

Recommendations …………………………………………………………………………………………………………………………38

References …………………………………………………………………………………………………………………………………….40

Control and management strategies for oak lace bug 1

Abstract

The oak lace bug Corythucha arcuata (Say) (: ) primarily feeds on species of oak (Quercus spp.) however, there are many other host plants that it is known to be associated with including some species of Castanea, Prunus, Malus, Rosa, Rubus, Ulmus, Acer, and . Oak lace bug is native to North America where it is not generally considered to be a because it is thought that natural enemies keep populations under check. When damage (caused by feeding) to host plants does occur it is usually only aesthetic.

Oak lace bug was first discovered in Europe () in 2000 but levels of damage, even now, are such that it is not considered to be a pest in this country. In 2003, oak lace bug was discovered in Turkey, and from here it has spread further into southern Europe and is now found in several countries. and the Republic of Croatia report rapid spread of the , and intense and severe attack in large areas of pedunculate oak forest. There is now growing concern, given the situation in the Republic of Croatia, that oak lace bug has the potential to become a serious primary pest of oak in favourable environments, causing considerable amounts of damage not only to the infested plants themselves but potentially also to the wider ecosystem.

Natural dispersal of this insect is slow because it is not a strong flyer. Most of the dispersal within Europe has been linked to anthropogenic activity, especially hitchhiking on transport (both road and rail). This is often associated with the movement of oak logs/timber from forested areas.

A range of are reported in the literature for the control of lace bugs however, issues with application often mean that either efficacy is poor or that certain active ingredients cannot be used. For instance, it is often not feasible to use spray applications (which must be directed at the underside of the leaves where the insect feeds) in forested areas, and many of the effective ingredients are classed as highly hazardous chemicals by the Forest Stewardship Council (FCS) and therefore prohibited from use in areas under FSC management. There are currently no biological control options for oak lace bug, and only limited research has been undertaken into such control measures.

There is a lot of uncertainty surrounding the impact that oak lace bug could have in the UK if it were to be introduced. It is clear these uncertainties should be addressed, and that control options should be given some consideration so that a fast response can be initiated should this insect be discovered.

Control and management strategies for oak lace bug 2

Chapter 1. Introduction

The Oak lace bug, Corythucha arcuata (Say) (Hemiptera: Tingidae), also known as Corythuca arcuata, is primarily considered to be a minor pest of numerous species of oak (Quercus) and some other species such as Castanea, Acer, Malus and Rosa (Pernek and Lacković, 2017). Life cycles and control measures for lace bugs in the Tingidae family are similar (UConn Home and Garden Education Center, 2016). In particular, (Say) the sycamore lace bug (the name ‘’ lace bug has been suggested to avoid confusion in Britain; Malumphy et al., 2007) has a similar biology to C. arcuata in that the adults also overwinter on the bark (of Platanus species). For this reason, control options and research relating to other Corythucha species has been included in this review when considered to be relevant.

1.1 Geographical distribution

Oak lace bug is native to North America where it is widespread (Rabitsch, 2008) and found in most states of the USA and also in southern Canada where it has a more limited distribution (EPPO, 2007; Pernek and Lacković, 2017). It is absent from Africa, Central and South America, and Oceania but is recorded as present in Asia (Iran (2005; Anderson, 2018)) and has invaded a number of countries within Europe (Pernek and Lacković, 2017; Anderson, 2018). The earliest record of its existence in Europe was in 2000 when it was found in Italy (in parks and along roads north of Milano, Lombardia and Piemonte); its existence in several areas indicated that it may have been present for some years (Bernardinelli and Zandigiacomo, 2000; 2001; EPPO Reporting Service 2001/057; EPPO, 2007; Pernek and Lacković, 2017).

Further first records have been recorded in other European countries: Turkey (2003; Mutun et al., 2009); (2002/3; Forster et al., 2005); (2012; Dobreva et al., 2013); Croatia (2013; Hrašovec et al., 2013); Hungary (2013; Csóka et al., 2013); Serbia (2013; Hrašovec et al., 2014; Pap et al., 2015); (2015; Chireceanu et al., 2017); Russia (2015; Neimorovets et al., 2017); Slovenia (2016; Jurc and Jurc, 2017); (2016; Csepelényi et al., 2017b; Berta et al., 2018); (2017; Alim’agri, 2017); Bosnia-Herzegovina (2017; Dautbašić et al., 2018), and most recently in (2018; Zúbrik et al., 2018) and (2018; Pernek and Lacković, 2017; Anderson, 2018). Csóka et al. (2017) indicate that the rate of spread across south has significantly increased in recent years; rapid spread and outbreaks were recorded in Hungary, Croatia, Serbia and Russia (Krasnodar region) during 2016, affecting thousands of hectares of oak forest (predominantly Q. robur).

Oak lace bug is currently absent from the UK with no recorded interceptions or outbreaks (Anderson, 2018).

1.1 Morphology and biology

Adults can be up to 4mm in length and are easily recognisable using the following brief description (Bernardinelli and Zandiagiacomo, 2001; Sancisi-Frey, 2017). The adults are whitish in colour with variable, irregular brown markings. The forewings and pronotum (middle part of the body) are expanded laterally forming a broadened lace-like covering of the body. The pronotum is inflated

Control and management strategies for oak lace bug 3

anteriorly into a bulbous ‘hood’ which covers the insect’s head. Small spines are present along the costal margin of the forewings, edges of the pronotum, and tip of the hood.

Adult oak lace bugs overwinter on or near their host in cracks and crevices of bark, branches, under leaf litter and other protected places (Csepelényi et al., 2017a; Pernek and Lacković, 2017; Sancisi- Frey, 2017; Simov et al., 2018). In Bulgaria, overwintering C. arcuata have been found under the bark and in bark crevices of the non-host species Scots pine (Pinus sylvestris L.) as well as on pedunculate oak (Quercus robur L. (Simov et al., 2018). Oak lace bug typically overwinters in groups although the size of the groups can be extremely variable (Csepelényi et al., 2017a). As soon as the leaves start to appear in the spring, the adults move on to them and start feeding, piercing the epidermis on the underside of the leaf and sucking out the cellular sap (Pernek and Lacković, 2017). After a month of feeding (Alim’agri, 2017), the females lay their eggs, which are brown-black, elongate in shape and approximately 0.5 mm in length (Anderson, 2018). Each female can typically produce 15 to 100 eggs or more (Pernek and Lacković, 2017). Eggs are laid on the underside of the leaves, often in clusters around the main leaf veins (Pernek and Lacković, 2017; Sancisi-Frey, 2017). The number of eggs in a cluster can be extremely variable (Csepelényi et al., 2017a). In Italy, clusters of 15 to 100 or more eggs are reported (Bernardinelli and Zandiagiacomo, 2001) while in Turkey an average of 49 (range of 12 – 120) eggs per leaf has been reported (Mutun et al., 2009), and 12 - 61 eggs per cluster reported from observations in Slovenia (Jurc and Jurc, 2017). Eggs hatch after a few days (Alim’agri, 2017). Development takes four to six weeks, passing through five nymphal stages in the process (Bernardinelli and Zandiagiacomo, 2001; Pernek and Lacković, 2017). The first four nymphal stages are reported to last two to three days each with a longer fifth nymphal (six to seven days) (Anderson, 2018). Nymphs do not have the characteristic lacy wings but can be recognised by their grey-black oval shape (up to 2 mm in length), presence of many spikes on the body, and from the third nymphal stage onwards white spots are also present on the body (Bernardinelli and Zandiagiacomo, 2001; Sancisi-Frey, 2017). The first generation of emerging adults are able to reproduce after a few days (Alim’agri, 2017). All life stages may be present on the underside of leaves at the same time (Sancisi- Frey, 2017). The presence of egg shells, nymphal exoskeletons and excrement (initially liquid droplets that harden into black spots) on the lower leaf surface are a further characteristic of lace bug infestation, and the nymphs are often clustered among this detritus (Pernek and Lacković, 2017; Sancisi-Frey, 2017). Barber (2010) reports that oak lace bug has a preference for trees growing under an open canopy but suggests that this may be due to the fact that fewer natural enemies were present in these habitats compared with shadier environments.

Oak lace bug can have two to three generations per year in its native range and damage to the tree increases with each generation (Rabitsch, 2008; Sancisi-Frey, 2017). Bernardinelli (2007) reports two complete generations per year and a partial third in the province of Milan (Italy) whilst Bernardinelli (2000) reports three generations, and an incomplete fourth in Italy where the climate is moderate. Berta et al. (2018) similarly report three to four generations per year in continental areas.

1.3 Host plants

The host plants of oak lace bug in its native North America are primarily species of oak: Quercus acuminata (Michx.) (also known as Q. muehlenbergii Engelm; chinkapin oak), Q. alba L. (white oak), Q. macrocarpa Michx. (bur oak), Q. prinoides Willd. (dwarf chinkapin oak), Q. prinus L. (chestnut oak), Q. rubra L. (red oak) and also Castanea americana (Michx.) (American chestnut; also known as C.

Control and management strategies for oak lace bug 4

dentata (Marshall); The Plant List, 2013). Oak lace bug is also occasionally reported on Acer, Malus, Pyrus and Rosa in North America (EPPO Rse 2001/057; Pernek and Lacković, 2017).

The most recent UK pest risk analysis (Anderson, 2018) has a detailed list of known host species in the invasive range of the pest, compiled from Csóka et al. (2017) and other literature, and the reader is referred to the PRA for detail. Briefly, host species reported in Europe on which oak lace bug symptoms are very common and often abundant include:

• Castanea sativa Mill. (sweet chestnut)

• Prunus serotina Ehr. (wild black cherry)

• Quercus (oak) spp. (Q. alba L. (white oak), Q. cerris L. (Turkey oak), Q. frainetto Ten. (Hungarian oak), Q. hartwissiana Steven (Strandzha oak), Q. libani G. Olivier (Lebanon oak), Q. pedunculiflora K. Koch (grayish oak), Q. petraea (Matt.) Liebl (sessile oak), Q. pubescens Willd. (downy oak), Q. robur L. (pedunculate oak), Q. virgiliana (Ten.) Ten (Virgil’s oak))

• Rubus caesius L. (European dewberry)

• Tilia cordata Mill. (small-leaved lime) and T. platyphyllos Scop. (large-leaved lime)

Host species reported in Europe, on which oak lace bug symptoms are common and sometimes abundant include:

• Quercus (oak) spp. (Q. macranthera Fisch. & C.A.Mey. ex Hohen (Caucasian oak), Q. pontica K. Koch (Armenian oak))

• Rosa canina L. (dog rose)

• Ulmus minor Mill. (field elm)

Host species reported in Europe on which oak lace bug symptoms are occasional or rare:

• Acer campestre L.1 (field maple) and A. laetum C.A.Mey (also known as A. cappaocicum Gled.; Cappadcian trees)

• Carpinus betulus L. (European/common hornbeam)

• Corylus avellana L. (common ) and C. colurna L. (Turkish hazel)

• Cotinus coggygria Scop. (European smoketree)

• Fagus sylvatica L. (European/common beech)

• Kerria japonica (L.) DC. (Japanese rose ‘Golden Guinea’)

• Koelreuteria paniculata Laxm. (golden rain tree)

• Lysimachia punctata L. (large yellow loosestrife)

• Malus sylvestris L. (European crab apple)

• Prunus avium L. (wild cherry), P. serrulata Lindl. (Japanese cherry), P. spinosa L. (blackthorn)

1 Bernardinelli (2006) laboratory study suggests that C. arcuata cannot develop on A. campestre.

Control and management strategies for oak lace bug 5

• Quercus ilex L. (evergreen oak), Q. imbricaria Michx. Not A.Gray ex A.DC (shingle oak), Q. macrocarpa (bur oak)

• Robinia pseudoacacia L. (black locust)

• Rubus ulmifolius Schott (wild blackberry)2

• Sorbus aria Crantz (whitebeam) and S. torminalis (L.) Crantz (wild service tree)

• Ulmus glabra Huds. (wych elm)

A laboratory study in Italy has also indicated that oak lace bug is capable of developing on Rubus ideas L. (raspberry). Mutun et al. (2009) observed adult lace bugs, and excrement, on hawthorns (Crataegus spp.) in Turkey but suggest that they were not feeding or laying eggs on these species as no eggs, nymphs or cast exoskeletons were found on the leaves.

In Croatia, the predominate hosts of oak lace bug are the pedunculate and sessile but feeding damage and nymphal stages have been observed on the European crab apple, Rubus spp. and the field elm. (Pernek and Lacković, 2017).

1.4 Symptoms of attack

Both adults and nymphs feed on the underside of the leaves and suck fluid from the cells between the upper and lower epidermis (Anderson, 2007; Pernek and Lacković, 2017). Initial symptoms of feeding damage are visible as a stippling of small yellow spots on the upper leaf surface, often around the leaf veins (Sancisi-Frey, 2017). As populations build the spots merge to create large areas of yellow or brown chlorotic colouration on the leaves (Sancisi-Frey, 2017). Usually, only minor aesthetic damage is observed on host plants in the native range (Anderson, 2007; Pernek and Lacković, 2017). In contrast, severe damage has been reported in parts of the invasive range (Csepelényi et al., 2017b; Berta et al., 2018; Franjević et al., 2018). Severe damage includes extensive chlorotic damage, summer yellowing of the leaves followed by browning of the foliage, premature leaf fall, reduced photosynthesis and sap flow, and desiccation (EPPO Rse 2001/057; Anderson, 2007; Rabitsch, 2008; Pernek and Lacković, 2017; Defra, 2018). Acorns from infested trees have been observed to fall earlier than expected in Croatia however, information on the effect that oak lace bug has on acorn yields is still speculative (Franjević et al., 2018). Anderson (2018) suggests there is some indication that acorn crops are negatively affected by severe infestations of the pest. Berta et al. (2018) report that the greatest damage in Croatia occurs in August due to the exponential growth of the populations, and that infested trees are not creating new wood during the late summer and are getting weaker. Heavy infestations and repeated attacks are likely to result in reduced growth and vigour of the trees leaving them more susceptible to other pests, secondary pest attacks, diseases and stresses (e.g. drought and pollutants) (EPPO Reporting Service 2001/057; Rabitsch, 2008; Pernek and Lacković, 2017; Anderson, 2018; Defra, 2018). Some authors have suggested that damage caused by oak lace bug could increase problems such as oak decline (Bernardinelli and Zandigiacomo, 2001; Bernardinelli 2006).

1.5 Dispersal

2 Fewer eggs are laid on R. ulmifolius compared with on Quercus species (Bernardinelli, 2006).

Control and management strategies for oak lace bug 6

It is thought likely that the current distribution of oak lace bug in southern Europe has come about through dispersal from the invasive population identified in Turkey in 2003 whilst the population in Switzerland is thought likely to have resulted from dispersal of the population identified in the north western region of Italy (Csóka et al., 2017).

Literature suggests that oak lace bug naturally spreads slowly (Anderson, 2018). The adults are not good fliers and move slowly (Pernek and Lacković, 2017). Medium to long distance travel is therefore due to wind, and to human assistance either by movement of infected trees for planting, wood and wood products, or by hitchhiking on transport (Mutun et al., 2009; Pernek and Lacković, 2017; Anderson, 2018).

Hitchhiking on transport (road or rail) has been identified as the probable means of dispersal in Italy (Bernardinelli, 2000), Turkey (Mutun et al., 2009), Croatia (Pernek and Lacković, 2017; Berta et al., 2018), Russia (Neimorovets et al., 2017), Slovenia (Jurc and Jurc, 2017), Hungary (Csepelényi et al., 2017a), Romania (Chireceanu et al., 2017) and Bulgaria (Dobreva et al., 2013; Simov et al., 2018). Csepelényi et al. (2017b) consider that the spread of oak lace bug is mainly passive, and that spread by road and rail is of the utmost importance because spread does not occur along an evenly moving frontline but manifests itself through smaller distant foci. In light of the more recent evidence from southern Europe, it is now thought that the pest can spread quickly with trade and transport. However, Anderson (2018) suggests that it is not clear what proportion of the spread observed in Croatia is down to the movement of logs, timber and woodchips or natural spread assisted by the movement of road traffic.

1.6 Pest Status

The arrival of oak lace bug in Italy prompted its addition to the EPPO Alert List in 2001 but it was subsequently deleted from the list in 2007 because an Italian pest risk assessment concluded that there were no efficient phytosanitary measures that could stop the natural spread of the pest (EPPO, 2007). Oak lace bug is not currently listed in the EC Plant Health Directive List of Invasive Alien Species of Union concern (“Union List”) under the EU Regulation No 1143/2014 on the prevention and management of the introduction and spread of invasive alien species (EU Regulation 2016/1141; EU Regulation 2017/1263). Neither is it recommended for regulation as a quarantine pest by EPPO although it is included on the Eurasian Economic Union (EAEU) A1 list 3. A Pest Risk Analysis for C. arcuata was originally drawn up for the UK in 2007 (Anderson, 2007). Concern that the pest may spread to the UK, along with increasing availability of information on its host range and impacts as it spreads across Europe, prompted the UK to revise its Pest Risk Analysis for C. arcuata in 2018 (Anderson, 2018). The pest has unmitigated and mitigated risk ratings of 60 on the UK Plant Health Risk Register, with statutory action indicated in the event of an interception; an action to raise awareness to encourage early detection in the event of an introduction is also indicated. In 2018 Defra issued a pest alert for oak lace bug (Defra, 2018) and is currently seeking to make the UK a protected zone for this species (Appleby, 2018).

Originally, information relating to the economic impacts of this pest was scarce; major economic damage was thought possible, but the evidence was lacking creating uncertainties over the levels of phytosanitary measures needed (Pernek and Lacković, 2017). However, as the pest has spread across

3 https://gd.eppo.int/taxon/CRTHAR/categorization

Control and management strategies for oak lace bug 7

Europe, and the levels of infestation have become more severe, there is growing concern that the oak lace bug will become an increasingly important pest in European oak forests (Csóka et al., 2017). Oak supports a very rich biodiversity with over 2000 species of mosses, lichens, fungi, invertebrates, birds and mammals associated with oak in the UK (SEFARI, 2018). Excluding the Nematocera, 801 species of invertebrates have been recorded on Q. petraea and 1149 species recorded on Q. robur in the UK (Southwood et al., 2005). It is not yet clear how large populations of oak lace bug, and the damage that they cause, will impact upon other insect communities on oak (Dobreva et al., 2013). This therefore creates uncertainty with regard to impacts on species that use oak for food and habitat (Anderson, 2018). Anderson (2018) concludes that greater evidence is now available to support potential effects of this pest such as greater potential environmental impact, albeit still with many uncertainties.

The possibility of potential associations with plant pathogenic fungi should also be considered. The sycamore lace bug C. ciliata is suspected to vector the plant pathogenic fungi (Ellis & Halsted) and veneta (Sacc. & Speg.), and that in combination with these fungi, causes the decline and death of trees (Malumphy et al., 2007). To date, there are no known associations of C. arcuata with plant pathogenic fungi but Anderson (2018) states that there is the possibility that it could come into contact with a pathogen in its invasive range that it has not previously encountered, and act as a vector for it.

Control and management strategies for oak lace bug 8

Chapter 2. Control options

Preventing the spread of oak lace bug is considered to be unachievable with currently available options of controlling this pest (Csóka et al., 2017; Pernek and Lacković, 2017; Anderson, 2018). Literature from the USA, where these bugs are native, and not generally considered to be a pest because they do not cause extensive harm to trees, forest ecosystems or industry, tends to give guidelines for lace bugs in general rather than for specific species; most of the information available is aimed at the home gardener or landscaper to minimise aesthetic damage. Such literature suggests that lace bug populations can be suppressed by spraying the underside of leaves with strong jets of water as soon as the eggs hatch, and if the tree is small it can control a light infestation; the jet knocks the nymphs off the foliage and they seldom make it back to the plant before they die (Dreistadt, 2014; UConn Home and Garden Education Center, 2016; Blake et al., 2018). However, whilst this method may suppress or control populations it is not likely to eradicate a population. It is also likely to need repeating on several occasions during the season and is only really practical in urban areas. If significant damage to plants occurs and suppression of oak lace bug is required in the USA, guidance indicates that plants should be monitored in subsequent years at a weekly interval from late winter so that action can be taken when the pest becomes abundant but before extensive damage occurs (Dreistadt, 2014).

2.1 Cultural control

In the USA, where damage caused by lace bugs is considered mostly aesthetic rather than injurious, correct cultural care of trees can be an option to alleviate the symptoms of attack. This includes measures such as growing plants that are well adapted to the site conditions, replacing poorly performing plants or those that repeatedly succumb to unacceptable levels of damage, ensuring good irrigation, and keeping the soil under host plants bare during the winter by raking up leaf litter to reduce numbers overwintering in the litter (Dreistadt, 2014). However, it should be noted that Sancisi- Frey (2017) consider that it is very important not to remove leaf litter, soil, wood or foliage from infested sites because of the risk of spreading the overwintering adults.

2.2 Removal and destruction of hosts

The most recent UK pest risk analysis for oak lace bug (Anderson, 2018) considers removal and destruction of infested trees as unlikely to be an effective means of eradicating and containing the pest because of its wide host range, and the range of materials that it could be present on (live wood and dead wood). Indeed, the PRA suggests that a removal and destruction approach may be more destructive than oak lace bug itself.

2.3 Chemical control

Many online sites (e.g. Krischik and Hahn, 2003; Malumphy et al., 2006; Krischik and Davidson, 2013; Dreistadt, 2014; UConn Home and Garden Education Center, 2016; Rosetta, n.d.) suggest a number of biorational, non-residual contact, insecticides for controlling lace bugs in the USA (i.e. measures that are relatively non-toxic to people and with few environmental side-effects):

Control and management strategies for oak lace bug 9

• • Horticultural oil (mineral oil/petroleum distillate) • Azadirachtin • Neem oil • Potassium phosphate • Pyrethrin products (often combined with piperonyl butoxide, which acts as a synergist)

Dreistadt (2014) suggest that almost any contact can be used to control lace bugs but as with forceful water sprays, repeated applications are likely to be necessary. Table 1 provides a list of the insecticides that have been/are currently used in the USA for control of lace bugs. They include active ingredients from a number of alternative classes including organophosphates, carbamates, pyrethroids, and the newer anthranilic diamides. With all spray applications, it is essential that good coverage of the underside of the leaves is obtained in order to get good control (UConn Home and Garden Education Center, 2016). Spray application should be conducted when the bugs are first observed but numerous (Dix et al., 1986; Krischik and Hahn, 2003; Krischik and Davidson, 2013).

Early literature from the USA suggests that the control measure for Corythucha spp. is to spray the lower surfaces of leaves with carbaryl, acephate or malathion. However, more recent literature from the USA does not recommend the use of broad-spectrum residual spray insecticides because of their high toxicity to natural enemies and pollinators, and because they can run off into surface water and drains leading to non-target effects on aquatic organisms (Dreistadt, 2014). Carbamates, the organophosphate malathion, and the pyrethroids bifenthrin, fluvalinate4 and permethrin should be avoided for these reasons (Dreistadt, 2014).

Systemic insecticides are also available for use against lace bugs in the USA (Dix et al., 1986; Krischik and Hahn, 2003; Krischik and Davidson, 2013; Dreistadt, 2014), and are included in Table 1. These can be applied by spray, soil drench or trunk injection however, soil application or trunk spray are advised whenever possible (Dreistadt, 2014). When applied correctly systemic insecticides such as Safari (active ingredient: ), Bayer Advanced Tree and Shrub Insect Control (Merit; ), and Lilly Miller Ready-to-Use Systemic, Orthene (active ingredient: acephate) may provide season long control (Dreistadt, 2014). However, systemic insecticides can be toxic towards other feeding on the tree, beneficial insects and pollinators. Pavela et al. (2013) report on a study whereby they injected azadirachtin (NeemAzal-U) into Plantanus sp. trees at rates of 0.1 and 0.05 g active ingredient per cm of diameter at breast height to investigate efficacy against the sycamore lace bug C. ciliata. Both rates resulted in substantial reductions in the mean number of C. ciliata present on the trees ranging from 4.9 – 29.1 in treated trees to 105.8 – 152.3 in the untreated trees.

Chlorantraniliprole, a newer insecticide belonging to the anthranilic diamide class of , is considered a potential replacement for neonicotinoids and pyrethroids because it is less harmful to non-target insects. It is the active ingredient in the Product Acelepryn, currently registered for use in the USA (US Environmental Protection Agency, 2019) to control lace bugs along with a considerable number of other pests. However, Redmond and Potter (2017) report poor efficacy when they compared one- and seven-day old foliar residues of chlorantraniliprole with bifenthrin against the related hawthorn lace bug (Fitch). Leaves were sprayed (hand sprayer) in the field at label rate (Acelepryn; 0.312 ml/L), and field-weathered before detaching from the tree and

4 Fluvalinate is now obsolete (PPDB, 2019).

Control and management strategies for oak lace bug 10

placing in Petri dishes in the laboratory to test residual activity against adults. Chlorantraniliprole proved to be ineffective at providing residual control of C. cydoniae whereas one- and seven-day old residues of bifenthrin gave 95% and 47% control, respectively (Redmond and Potter, 2017). The authors suggest that the observed ineffectiveness of chlorantraniliprole was due to its relatively low systemicity in plants. It is worth noting here that bifenthrin has previously proved efficacious at eradicating an outbreak of C. ciliata in the UK. In 2006, an outbreak was detected on imported plants at two nurseries in Bedfordshire, UK, and in the surrounding locality of one of the nurseries on trees growing in a hedge 50 metres away (Malumphy et al., 2007). Infested trees were sprayed with bifenthrin, and this successfully eradicated the pest despite the fact that the trees were large; the pest was subsequently declared absent following treatment and no further findings (Anderson, 2018).

It should be noted however, that Forest Stewardship Council (FSC) standards currently prevent the use of ‘highly hazardous’ chemical insecticides in forest areas and promote non-chemical methods of pest management as an element of an integrated pest management strategy (FSC-STD-GBR-03-2017; FSC-POL-30-001-2005; Anderson, 2018).

A further newer , bistrifluron, is an example of the benzoylphenylurea (BPU) class of insecticides and acts by inhibiting chitin synthesis. Whilst there is no mention in the literature or online sources of this insecticide being used to control lace bugs, a laboratory trial has indicated good potential for controlling C. ciliata (Changmann et al., 2008). These authors used leaf dip assays to assess larvicidal and ovicidal activity as well as adult mortality and fecundity. Larvicidal activity was measured five days after placing on dipped leaves with all nymphal stages; LC 50 values ranging from 0.01 – 0.06 ppm are given (Changmann et al., 2008). When fifth instar nymphs were placed on leaves dipped in 10 ppm and 100 ppm bistrifluron solutions, the proportion of them reaching adulthood was significantly reduced (63% and 41.4%, respectively, compared with a control value of 93.3%) although the lower concentrations of 1 and 0.1 ppm had no significant effect. Furthermore, adult longevity was also reduced (when treated during the fifth nymphal instar) compared with non-treated individuals (longevity 38.5 days) such that those exposed to leaves dipped in a 0.1 ppm solution survived for 11.9 days whereas those exposed to leaves dipped in a 100 ppm solution survived just 2.8 days (Changmann et al., 2008). The fecundity of the surviving females was also much reduced; those in contact with the two highest doses tested (10 ppm and 100 ppm) did not lay any eggs (Changmann et al., 2008). When adult insects were subjected to bistrifluron, longevity was similarly reduced with increasing dose (10 – 100 ppm) as was the length of the preovipositon period; 100 ppm more than doubled the preoviposition period from 7 days (control insects) to 15.6 days whilst the insects subjected to leaves dipped in a 1 ppm solution required a 10-day oviposition period. Treated adults laid significantly fewer eggs with increasing dose, and these eggs had a significantly reduced hatch rate with increasing dose (Changmann et al., 2008). However, ovicidal activity per se was not observed when leaves which had eggs already laid on them were dipped in bistrifluron although all the larvae died within 24 hours of hatching when concentrations of 1 – 100 ppm were used; 70-80% mortality of hatched nymphs was observed when a concentration of 0.1 ppm was used depending on the age of the egg at the time of treatment (Changmann et al., 2008).

Whilst the active ingredient bistrifluron is not currently approved for use in the EU, a number of other BPU active ingredients are commercially available and approved in the EU including diflubenzuron, triflumuron and lufenuron. In the UK, Dimilin Flo (active ingredient: diflubenzuron) is authorised for use including in forest environments (subject to valid derogation according to FSC-PRO-30-001 V1-0 EN, 2014).

Control and management strategies for oak lace bug 11

Only one published investigation into the efficacy of plant essential oils against lace bugs was available at the time of writing. Rojht et al. (2009) compared the efficacy of thujone and essential oil of rosemary against larvae and adults of C. ciliata with the efficacies of deltamethrin and imidacloprid. The authors chose these products because rosemary oil has previously been reported to act as an insect repellent, a contact insecticide, and to reduce feeding and oviposition; thujone (an active component of essential oils) can have a repellency action against insects; deltamethrin and imidacloprid are recommended for use in some countries to control the sycamore lace bug (Rojht et al., 2009). Leaf dip or direct contact (via spray application) laboratory assays were performed. Deltamethrin and imidacloprid were the most effective; the recommended rate of deltamethrin caused 100% mortality of both larvae and adults, and the recommended rate of imidacloprid resulted in 89.6% and 59.1% larval and adult mortality, respectively. Interestingly, 1% concentrations of essential oil of rosemary and thujone were as equally effective as imidacloprid against larvae (83.6% and 88.1%, respectively) and adults (81.7% and 76.2%, respectively) (Rojht et al., 2009). The authors conclude that thujone and rosemary oil could be sprayed to the bark in autumn to help suppress overwintering populations.

Sycamore lace bug is also known to be highly susceptible to imidacloprid, and this is delivered most effectively by tree injection (Blake et al., 2018; CABI, 2018; Elmsavers, 2019). Other active ingredients recommended for the sycamore lace bug include acephate, dinotefuran and horticultural oil (Blake et al., 2018). Unfortunately, there are currently no authorised products containing imidacloprid, acephate or dinotefuran registered for use in the UK (The Pesticides Register Database). Imidacloprid is also effective against the hawthorn lace bug (C. cydoniae) (Gill et al., 1999; Szczepaniec and Raupp, 2007) and the cotton/bean lace bug C. gossypii (Fabricius) (90.37% efficacy after seven days), as is the organophosphate dimethoate (86.14% efficacy after seven days) whereas + lambda- cyhalothrin, spinetoram, malathion and thiamethoxam were not particularly so (0%, 21.46%, 38.77% and 50.84% efficacy after seven days, respectively) (Varon et al., 2010).

Control and management strategies for oak lace bug 12

Table 1. Summary details of the active ingredients used to control lace bugs (Corythucha spp.) in the USA. Information on authorisation status is taken from PPDB (2019), BPDB (2019), the EU Pesticides Database and the Pesticides Register of UK Authorised Products. NB. Whilst some of these active ingredients are approved for use in the UK, there are currently no products authorised for use on oak trees to control oak lace bug. Forest Stewardship Council (FSC) status is taken from the FSC list of ‘highly hazardous’ pesticides (FSC-STD-30-001a EN, 2017); this updated version of the list identifies the active ingredients that currently do not require a valid derogation for their use.

Insecticide Class Active ingredient Mode of action Approved in EU? Authorised products Forest Stewardship Council status in UK? Organophosphate Acephate Contact and No No Included in the FSC list of highly hazardous ingestion systemic pesticides. Active ingredient does not action require a valid derogation for use Chlorpyrifos Non-systemic with Yes Yes Included in the FSC list of highly hazardous contact, inhalation pesticides. Derogation according to FSC- and stomach action PRO-30-001 V1-0 is required before use Malathion Non-systemic with Yes No Included in the FSC list of highly hazardous contact, inhalation pesticides. Active ingredient does not and stomach action require a valid derogation for use Carbamate Carbaryl Contact and stomach No No Included in the FSC list of highly hazardous action with slight pesticides. Derogation according to FSC- systemic properties PRO-30-001 V1-0 is required before use Pyrethroid Bifenthrin Contact and stomach Yes No Included in the FSC list of highly hazardous action pesticides. Active ingredient does not require a valid derogation for use Cyfluthrin Non-systemic with No No Included in the FSC list of highly hazardous contact and stomach pesticides. Derogation according to FSC- action PRO-30-001 V1-0 is required before use Deltamethrin Non-systemic with Yes Yes Included in the FSC list of highly hazardous contact and stomach pesticides. Derogation according to FSC- action PRO-30-001 V1-0 is required before use

Control and management strategies for oak lace bug 13

Fluvalinate5 - - - - Lambda-cyhalothrin Non-systemic with Yes Yes Included in the FSC list of highly hazardous contact and stomach pesticides. Derogation according to FSC- action and repellent PRO-30-001 V1-0 is required before use properties Permethrin Non-systemic with No No Included in the FSC list of highly hazardous contact and stomach pesticides. Derogation according to FSC- action, slight PRO-30-001 V1-0 is required before use repellent effect Dinotefuran Systemic with No No Not included on FSC list of highly translaminar activity hazardous pesticides and with contact and stomach action Imidacloprid Systemic with Yes No Included in the FSC list of highly hazardous translaminar activity pesticides. Active ingredient does not and with contact and require a valid derogation for use stomach action Tetranortriterpenoid Azadirachtin Contact and systemic Yes Yes Not included on FSC list of highly hazardous pesticides Anthranilic diamide Chlorantraniliprole Primarily through Yes Yes Included in the FSC list of highly hazardous ingestion, pesticides. Active ingredient does not secondarily by require a valid derogation for use contact

5 Fluvalinate is obsolete (PPDB, 2019).

Control and management strategies for oak lace bug 14

2.4 Entomopathogenic fungi

Only two studies, both laboratory based, report on the potential control of C. arcuata using entomopathogenic fungi. The first study (Sönmez et al., 2016) was a preliminary screen of ten entomopathogenic fungi against both nymphs and adults of oak lace bug. Four isolates of Metarhizium anisopliae sensu lato, three isolates of (Bals,) Vuill, one isolate of Beauveria pseudobassiana S.A. Rehner & R.A. Humber, and one isolate of Myriodontium keratinophilum Samson & Polon were tested. In all cases a 1x 107 mL-1 concentration of conidial suspension was sprayed onto the insects, which were then kept on oak leaves collected from the field. The authors report that all isolates were able to infect, kill and initiate mycosis in both nymphs and adults of oak lace bug but with varying degrees of mortality (approximately 50 - 80% mortality of nymphs, and 55 – 90% mortality of adults within 14 days). The most effective isolate was B. bassiana KTU-24 with 80% mortality observed for nymphs and 90% mortality observed for adults within 14 days of application. This strain also achieved the highest mycosis values (76% and 83% for nymphs and adults, respectively (Sönmez et al., 2016)). Two isolates of M. anisopliae (KTU-2 and KTU-60) achieved good mortality of nymphs (70%) and adults (83%) over the same time period.

Further screening of B. bassiana strain KTU-24 was conducted to estimate LC50 values; during these further investigations (same experimental set up), 100% mortality of nymphs was achieved using conidial concentrations of 1 x 108 mL-1, and above, whilst a concentration of 1 x 109 mL-1 was required 7 6 to achieve 100% adult mortality (Sönmez et al., 2016). LC50 values of 1.17 x 10 and 6.44 x 10 conidia mL-1 were estimated for nymphs and adults, respectively.

Beauveria bassiana strain KTU-24 was initially isolated from the pine processionary Thaumetopoea pityocampa (Den. & Schiff.) (Sevim et al., 2010a) and showed the highest level of virulence against this insect when compared with a selection of B. bassiana strains isolated from this insect; 100% mortality within 10 days of application when third instar larvae were dipped into a suspension of 1 x 105 conidia mL-1. The same strain of B. bassiana is also reported to be effective against C. ciliata (Sevim et al., 2013; see below) and both the larvae and adults of European spruce bark Dendroctonus micans (Kug.) (Coleoptera: Curculionidae) achieving 96% and 56% mortality, respectively in laboratory bioassays (Sevim et al., 2010b). These studies would suggest that B. bassiana strain KTU-24 is therefore not specific to the hemipteran Tingidae and is capable of infecting and killing species in other insect Orders (Lepidoptera and Coleoptera), a factor that must be considered when selecting entomopathogenic fungi for use in biological control programmes.

Information on the second study regarding efficacy of entomopathogenic fungi towards C. arcuata is minimal, with only an abstract for a conference poster available (Matek and Pernek, 2018). The abstract indicates that 51% mortality was achieved within one week of B. bassiana conidial suspension application to adult oak lace bugs that had been placed in moss in a laboratory trial, thus mimicking one known overwintering habitat. The authors also report a mycosis value of 47%. However, no further information is given, including for example, the strain of B. bassiana used, the concentration of the conidial suspension applied, or the environmental conditions (temperature, humidity) used during the experiment.

Screening of entomopathogenic fungi against related species of lace bugs, in particular C. ciliata, has been reported by a number of authors (Sevim et al., 2013 and references cited within). The most recent of these studies (Sevim et al., 2013) was conducted by the same group of researchers who

Control and management strategies for oak lace bug 15

screened for efficacy of the entomopathogenic fungi against oak lace bug, using the same methodology (except that insects were kept on plane leaves instead of oak leaves); they tested four isolates of B. bassiana, two isolates of B. pseudobassiana, six isolates of M. anisopliae and one isolate of Wize (formerly Paecilomyces farinosus) against both nymphs and adults. As with oak lace bug, the B. bassiana isolate KTU-24 appeared to have the greatest efficacy against C. ciliata with 86% mortality observed within 14 days of application for both nymphs and adults. The same strain also exhibited the highest level of mycosis (80% and 83% for nymphs and adults, respectively). Two strains of M. anisopliae also achieved high mortality against adults (strain KTU-60: 86% and strain KTU-2: 83%) but lower mortality (approximately 65-70%) against nymphs. In contrast, it was the KTU- 27 strain of M. anisopliae that conferred the second highest level of mortality (80%) in nymphs. One strain of B. bassiana and two strains of M. anisopliae were not effective at killing adult C. ciliata however, the remaining strains achieved mortalities of 43-86% in adults. In addition to the three strains that were ineffective against adults, a further strain of B. bassiana and both strains of B. pseudobassiana were found to be ineffective against the nymphs. The remaining effective strains caused larval mortalities in the range of 36 – 73%. Further screening of B. bassiana strain KTU-24 was conducted (Sevim et al., 2013). A concentration of 1 x 108 conidia mL-1 killed all nymphs and adults 5 -1 within 14 days of application, and LC50 values were estimated to be 3.96 x 10 conidia mL and 5.51 x 105 conidia mL-1, respectively.

Sevim et al. (2013) go on to discuss their findings in relation to work previously reported in the 1980s by other authors investigating the efficacy of entomopathogenic fungi against C. ciliata (original publications unavailable at time of writing). It would appear from this discussion that of all the species of fungi investigated (B. bassiana, Verticillium lecanii (Zimmerman) (now known as lecanii R. Zare & W. Gams), I. fumosorosea), B. bassiana is the more efficacious species both in terms of pathogenicity and observed mortality rates. Infection rates of 10- 31% are quoted and up to 100% mortality observed. Beauveria bassiana is also the species most frequently isolated from overwintering adults although not necessarily the most virulent. One of these studies (Ozino and Zeppa (1988) reported and referenced within Sevim et al., 2013) included a field trial that resulted in 25% mortality of adults overwintering on trees following treatment with B. bassiana. A more recent study by Tarasco and Triggiani (2006) showed that a commercial strain of B. bassiana (Agrimport EXP 102®) had field efficacy. The was used at a concentration of 10 000 spores/ml and a 1500 ml suspension was sprayed using a hand sprayer from soil level to a height of 2 m onto each tree, which were 60-100 cm in diameter. Mortalities of 47.7% and 60%, recorded across the two trial sites after 14 days, were attributed to B. bassiana. Sevim et al. (2013) also cite a study in which a spray application of I. fumosorosea resulted in > 50% reduction in overwintering adults. Most of the reported work has used strains of fungi isolated from areas where the pest is present. Sevim et al. (2013) explain the rationale behind this focus: locally isolated strains may be more ecologically compatible with the pest species (in terms of geographical location and habitat type) and may also have a reduced risk of impacting on non-target organisms.

CABI (2018) lists the following entomopathogenic fungi as natural enemies of sycamore lace bug: Alternaria alternata (Fr.) Keissl.; B. bassiana; Fusarium oxysporum Schltdl.; L. lecanii; I. fumosorosea and the entomopathogenic strain of Mucor hiemalis Wehmer, suggesting that they may be used in Italy for biological control. However, no reference details are provided with this information and A. alternata, F. oxysporum and M. hiemalis do not appear to be approved active ingredients in the EU, and approval for Fusarium sp. L13 is pending (EU Pesticides database, 2019).

Control and management strategies for oak lace bug 16

Whilst L. lecanii (= L. muscarium strain Ve6) is an approved active ingredient in the EU it does not appear to be authorised for use in Italy (EU Pesticides database, 2019), and its intended use in countries where it is authorised is for greenhouse protected crops to control whitefly and , with an envisaged use in the field on strawberry (EC Review Report revision, 2014a). Similarly, I. fumosorosea Apopka strain 97 is an approved active ingredient in the EU but it does not appear to the authorised for use in Italy (EU Pesticides database, 2019), and its intended use in countries where it is authorised is for greenhouse protected crops (EC Review Report, 2014b). Six strains of B. bassiana are approved for use in the EU (EU Pesticides database, 2019) but only two (ATCC 74040 and GHA are authorised in Italy) and their intended use is on indoor or glasshouse crops (EC Review Report, 2014c and 2014d). Whilst the scientific literature reports on some field experiments trialling the use of entomopathogenic fungi against C. ciliata and suggests that they have the potential for helping to control populations, it is unclear whether they are now routinely used in biological control programmes for this pest.

2.5 Entomopathogenic nematodes

There does not appear to be any published work reporting on the use of entomopathogenic nematodes against the oak lace bug; however, the use of entomopathogenic nematodes to suppress populations of C. ciliata has been investigated by scientific researchers.

As part of the Tarasco and Triggiani (2006) field study mentioned previously, some trees were sprayed with entomopathogenic nematodes rather than B. bassiana to test efficacy against sycamore lace bug. Two species of nematodes were used: Steinernema carpocapsae (Weiser) (strain ItS-MR7) and Heterorhabditis bacteriophora (Poinar) (strain ItII-MRS), both previously isolated from Italian soil samples. Suspensions of 1000 infective juveniles (IJs)/ml (volume 1500 ml) were sprayed using a hand sprayer from soil level to a height of 2 m onto each tree, which were 60-100 cm in diameter. However, mortalities attributed to the entomopathogenic nematodes were disappointingly low (approximately 5% for both species after 14 days) considering that in a previous laboratory test C. ciliata had been more susceptible (Tarasco and Triggiani, 2006). Shapiro-Ilan and Mizell (2012) suggest that these applications may have failed to control C. ciliata because of environmental conditions, which are known to limit efficacy of entomopathogenic nematodes if not correct.

A laboratory evaluation of the efficacy of entomopathogenic nematodes against C. ciliata was reported upon in 2012 by Shapiro-Ilan and Mizell. These authors used leaf dip assays to assess the virulence of five different species of nematodes (all laboratory strains): H. bacteriophora (strains Baine and Oswego); Heterorhabditis indica Poinar Karunakar and David (HOM1 strain); Heterorhabditis georgiana Nguyen, Shapiro-Ilan and Mbata (Kesha strain); S. carpocapsae (Weiser (All strain) and S. riobrave Cabanillas, Poinar and Raulston (355 strain). Approximately 1600 infective juveniles (ca. 25 IJs per cm2) were applied to petri dishes in which leaf discs were held in agar, and once dried adult C. ciliata were added. Mortality was recorded after two days of incubation and a proportion of the infected bodies were analysed to obtain information on the reproductive capacities for each strain of nematode. All but one strain, H. bacteriophora (Oswego), caused significant mortality when compared with the control group (ranging from approximately 30-70% compared with control mortality of approximately 15%). Heterorhabditis indica (HOM1 strain) caused the greatest mortality (ca. 70%) and this strain also exhibited the highest reproductive capacity in C. ciliata producing just under 300 IJs per insect; reproductive capacities for the other strains were considerably lower (0 – 55 IJs per insect)

Control and management strategies for oak lace bug 17

(Shapiro-Ilan and Mizell, 2012). The authors therefore concluded that of all the strains tested, H. indica (HOM1 strain) showed the greatest potential for suppressing C. ciliata.

More recently still Verfaille et al. (2015) report on “The Protection of Border Tree Environment and Technology, 2008 - 2012 (PETAAL) program: a biocontrol strategy of the sycamore lace bug in urban areas”. Previous laboratory and field work within this program had identified that entomopathogenic fungi (Steinernema spp.) could significantly reduce the population of adult C. ciliata on the trunk and spring populations on the foliage (Verfaille et al., 2011); also, that the generalist predator Chrysoperla lucasina (Lacroix) (: ) fed mainly on larvae rather than adults, with a medium to high rate, and that it was able to effectively disperse in the tree (Verfaille et al., 2015). The project culminated with the design of a biocontrol strategy in which these agents were used in combination in an attempt to (i) reduce the overwintering adult population on the bark before it migrated to the foliage in the spring (ii) control the population growth on the spring foliage and (iii) reduce the population peak in the summer. Trials were conducted in six French cities with varying climatic conditions (although data from only four were analysed due to climatic conditions being unfavourable for population development during the year of the trial). Plane trees with a trunk height of approximately 5m and a comparable architecture were used and four treatments were applied during the season: (i) 7500 IJs/ml application of S. feltiae) on the trunk before migration when the required climatic conditions were met; (ii) foliar application of 7500 IJs/ml S. carpocapsae just after migration to the foliage; (iii) a release of C. lucasina eggs into the foliage six weeks after the end of migration (four or eight tubes, each one containing 120-150 eggs, depending on the tree height, volume of foliage and level of infestation; (iv) foliar application of 7500 IJs/ml S. carpocapsae when the populations were due to peak and lead to public nuisance issues (Verfaille et al., 2015). Note, S. carpocapsae was used in the two later entomopathogenic nematode releases because it is more suited than S. feltiae to the summer climate. Before application of any treatment, the overwintering populations of adults were approximately 80-90 individuals per dm2 of bark and consistent between the untreated and treated groups. Within one week of the first treatment (bark application of S. feltiae), a significant mean reduction in lace bug populations of 60% was observed although the variability in the reduction was quite high between the sites (33-75%). Effects of the second entomopathogenic nematode application were less immediate: no differences in populations levels observed after one week but a significant 50% reduction observed after three weeks (Verfaille et al., 2015). With the exception of one site, where a population reduction of 50% was observed following release, C. lucasina did not generally reduce populations of lace bug during the trial. The effects of the final nematode application could not be evaluated because a decrease in population levels was observed at the time when levels were expected to peak (Verfaille et al., 2015). The authors of the study concluded that just one trunk application of S. feltiae aimed at the overwintering adult population was effective at reducing adult populations and that moreover, it is a relatively inexpensive control method that can be easily applied but that determination of the optimal date for application, and climatic conditions at the time of application, would be crucial to its success. Whilst the first foliar application of nematodes was a success, the authors hypothesised that the efficacy of the predator may have been disappointing due to weather conditions, too low a predator/prey ratio or a negative interference between the predator and nematodes (although the timing between nematode application and release of the predator had been designed to take this into account).

2.6 Natural predators

Control and management strategies for oak lace bug 18

Natural enemies cannot be relied upon for complete control of lace bugs as their population levels do not build up sufficiently until the lace bug population has reached high levels (Dreistadt, 2014). However, when the lace bug population is not too large, natural enemies may be a good method for keeping them in check as is thought to be the case in North America (UConn Home and Garden Education Center, 2016) and so it is important to preserve levels of any natural enemies as part of a more long-term integrated measure (Dreistadt, 2014).

Lace bugs in the USA have several native natural predators that help to keep populations under control (UConn Home and Garden Education Center, 2016) including predatory assassin bugs, lacewing larvae (e.g. green lacewing Stephens), ladybirds, syrphid (hoverfly) larvae, jumping spiders, pirate bugs (), mirid (capsid) bugs and mites (references within Bernardinelli and Zandigiacomo 2001; Dreistadt, 2014; Blake et al., 2018; Anderson, 2018). The plant bugs include the mirids (Say) and Deraeocoris nebulosus (Uhler) (neither of which are found in the UK) and the anthocorid insidiosus (Say) (not native to the UK) (Wheeler et al., 1975; references cited in Anderson, 2018). In laboratory trials, Wheeler et al. (1975) demonstrated that D. nebulosus nymphs were capable of consuming an average of 107.6 oak lace bug larvae during their own nymphal development. It is not known whether any of the predatory species native in the USA would be suitable for release in the UK but generalist predators (such as H. vitripennis, D. nebulosus and O. insidiosus) are unlikely to be suitable (Anderson, 2018). Several species have been observed to predate upon oak lace bug nymphs and adults in Italy including spiders (Theridiidae, Tomisidae, Clubionidae, Salticidae), mites (Anystidae, Trombidiidae), Dermaptera (Forficulidae), (, , Anthocoridae) and Neuroptera (Chrysopidae) (Bernardinelli and Zandigiacomo, 2001).

2.6.1 Neuroptera

Larvae of the Neuroptera are entirely predacious (Chinery, 1973). The common green lacewing C. carnea is one of 18 species of green lacewing that occur in the UK (CABI, 2018; National Insect Week, 2019) and is also available from biocontrol companies (BPDB, 2019). It is listed as a natural enemy used for the biological control of C. ciliata in Italy however, it is very polyphagous (CABI, 2018) and is not particularly associated with oak.

The Checklist of British lacewings and their allies (Neuroptera, Megaloptera, Raphidioptera and Mecoptera) (Plant, 1997 accessed via Natural History Museum website) lists 68 species as present in Britain but only a few have an association with deciduous trees (or oak, in particular). Cunctochrysa albolineata (Killington) is a green lacewing associated with deciduous trees and is fairly frequent and widespread in Britain (NatureSpot, 2019). Nineta flava (Scopoli) is another fairly common and widespread species of green lacewing that can be found in wooded areas and thought to be associated with oak (NatureSpot, 2019). capitata (Fabricius), although typically associated with pine, has been recorded on oak trees however, although widespread in Britain populations are only local (NatureSpot, 2019). humulinus (Linnaeus) and H. lutescens Fabricius are species of brown lacewing that are quite common in Britain and have known associations with deciduous woods; Hemerobius micans Olivier is especially associated with mature oak but feeds on (NatureSpot, 2019). Drepanepteryx phalaenoides (Linnaeus), also a brown lacewing, is described as associated with woodlands (Lacewings and Allies Recording Scheme, 2019) but no information is given as to which plants/trees it is associated with.

Control and management strategies for oak lace bug 19

Two species of waxfly (Neuroptera: ), Parasemidalis fuscipennis (Reuter) and Semidalis aleyrodiformis (Stephens) have been recorded on both oak and pine, although S. aleyrodiformis is also associated with pine as an adult and prefers open and sunny habitats; both are widespread in England, but populations are local (NatureSpot, 2019). Snake flies (Raphidioptera; previously Neuroptera: Raphidiidae) are also predatory insects. Both Phaeostigma notata (Fabricius) and Xanthostigma xanthostigma (Schummel) spend most of their time high up in trees (emerge from May onwards) but the larvae live under loose bark and feed on other insects (X. xanthostigma has a preference for oak) (NatureSpot, 2019); these species are probably fairly common and widespread in England but are thought to be under recorded.

2.6.2 Hemiptera

The Checklist of Heteroptera of the British Isles (with Channel Isles) lists a number of anthocorid species as present in the British Isles (Nau, 2007) but none are listed as associated with oaks in the BRC Database of Insects and their food plants (2019). Five species of Orius (O. laevigatus (Say), O. laticollis (Reuter), O. majusculus (Reuter), O. niger (Wolff), and O. vicinus (Ribaut)) are recorded as present in the British Isles (Nau, 2007; CABI, 2018; BPDB, 2019; NBN Atlas, 2019). Orius laevigatus and O. majusculus are available from biocontrol companies for use in protected vegetables and ornamentals to control thrips although they will eat other insects such as aphids and mites, and the eggs of some lepidopteran species (BPDB, 2019). Both O. majusculus and O. vicinus are recorded as natural enemies of the related C. ciliata (CABI, 2019) in Italy (along with O. horvathi and O. insidiosus). Anthocoris nemoralis, another natural enemy associated with biological control of C. ciliata in Italy (CABI, 2018) is associated with many different species of deciduous tree and is widespread and frequent in the UK (NatureSpot, 2019). It feeds on mites, aphids, psyllids and thrips and is sold as a biocontrol agent (BugGuide, 2019; BPDB, 2019).

Species belonging to the Miridae family largely feed on plant tissues and some are serious plant pests, however, a few species within this family are partially predatory (Southwood and Leston, 1959). Hyaliodes vitripennis is one such species but is not present in the UK indeed, there are no species of Hyaloides listed as present in the British Isles (Nau, 2007). Hyaliodes vitripennis has been investigated for use as a biological control agent in apple orchards to control mites and aphids and was shown to significantly repress European red mite and two-spotted populations (Chouinard et al., 2006). The BRC Database of Insects and their Food Plants lists 28 species of Miridae associated with Quercus oak but only two (Psallus perrisi (Mulsant & Rey) and P. variabilis (Fallen)) are associated with Q. petraea and four (P. perrisi, P. variabilis, P. quercus (Kirschbaum) and P. wagneri Ossiannilsson) are associated with Q. robur. None of these four species appear to be predatory (Southwood and Leston, 1959). However, there are other species of Miridae present in the British Isles with predatory tendencies that Southwood and Leston (1959) report as associated with deciduous trees as listed in Table 2.

Himacerus apterus (Fabricius), known as the tree damsel bug, is the only UK species belonging to the Nabidae family of bugs that lives in trees, being found in deciduous trees and to a lesser extent on conifers (Table 2). Nabis pseudoferus Remane is listed as a natural enemy used for biological control of C. ciliata in Italy (CABI, 2018), and in the laboratory it is a very effective predator of C. ciliata, consuming 15 prey per day (Maceljiski and Balarin, 1977). However, it has only very limited distribution in the UK (NBN Atlas, 2017).

Control and management strategies for oak lace bug 20

Table 2. Species of Miridae and Nabidae bugs that have predacious/partly predacious feeding habits, known to be present in the British Isles and associated with oak or deciduous trees. In addition to the listed species found by Audsley et al. (2018) these authors also found other predatory Heteroptera in their oak samples: Arocatus longiceps, Bleparidopteris sp., Orthotylus nassatus, (Miridae); Elasmucha grisea (); Anthocoris sp. (Anthocoridae); Pentatoma rufipes () and Empicoris sp. ().

Family Species UK distribution Feeding preference Biology Host plant Reference

Miridae Deraeocoris flavilinea Common across south Listed as a natural Adults present June to Sycamore and field British Bugs (A. costa)6 and central Britain enemy used in July maple but frequently (2018); CABI biological control of C. found on other trees (2018) ciliata in Italy and shrubs Miridae Deraeocoris lutescens England and Wales Small insects but may Overwinters as an adult, Oak, hazel and other Southwood and (Schilling)7 (south of a line from also probe leaves. eggs laid late May and trees Leston (1959); the Wash to Cardigan Listed as a natural June, larvae present mid- CABI (2018) Bay) enemy used in June until early October biological control of of C. ciliata in Italy Miridae Phylus Throughout the Adults are partly Overwinters as eggs, Oak Southwood and melanocephalus (L.) British Isles predacious larvae hatch mid-May, Leston (1959) adults present mid-June to early August Miridae Psallus varians Common across UK Adults and larvae Adults present May to Oak British Bugs (Herrich-Schäffer) feed on small insects August (2018); as well as the host NatureSpot trees (2019) Miridae Campylomma South east England Feeds on plants but is Two generations per year; Several plants but Southwood and verbasci (Meyer-Dür) also an important first generation adults are includes oak Leston (1959) predator of red spider present in June, the mites, thrips, aphids second generation adults

6-6 These species were found on Q. robur that were sampled in a previous Future Proofing Plant Health project (Audsley et al., 2018).

Control and management strategies for oak lace bug 21

and other small are present August to insects. Larvae are October also partly predacious Miridae Campyloneura Throughout the Larvae and adults Overwinters as eggs Wide variety of trees, Southwood and virgula (Herrich- British Isles exhibit predacious which hatch May to June. especially hawthorn, Leston (1959) Schäeffer)8 feeding on red spider Adults present July to hazel and oak mites, eggs and larvae October of bark lice and aphids (also recorded feeding on ) Miridae Pilophorus perplexus9 South of a line from Feeds on aphids, Eggs hatch May to June, Oak and other Southwood and Douglas and Scott the Wash to other small insects adults present July to deciduous trees Leston (1959) Glamorgan and moth eggs October Miridae Cyllecoris histrionicus Widespread Larvae and adults Overwinters as eggs Common on oak Southwood and (L.) throughout the British feed on unopened which hatch in mid-May, Leston (1959); Isles catkins and very adults present mid-June British Bugs young acorns but to mid-July (2018) largely predacious on aphids, psyllids, bark flies and larvae within Spangle galls Miridae Dryophilocoris All parts of the British Larvae and adults Larvae hatch in May, Common on oak Southwood and flavoquadrimaculatus Isles feed on unopened adults present at end of Leston (1959) (De Geer) catkins and other May to end of June parts of oak as well as on aphids, small flies, insect eggs and other mirid larvae

8-8 These species were found on Q. robur that were sampled in a previous Future Proofing Plant Health project (Audsley et al., 2018).

Control and management strategies for oak lace bug 22

Miridae Orthotylus tenellus Widely distributed Feeds on catkins but Eggs hatch in spring, Ash, oak and hazel but Southwood and (Fallén) throughout the British also on aphids, adults present late June especially ash Leston (1959) Isles whitefly, small flies, to August eggs and young larvae of and Miridae Lygocoris viridis Widely distributed Feeds on flowers and Eggs overwinter and Common on lime but Southwood and (Fallén) throughout the British fruits but also attacks hatch in May, adults also occurs on , Leston (1959) Isles aphids and psyllids present towards the end buckthorn and oak of June to September Miridae Miris striatus Throughout the Adults and larvae are Eggs overwinter and Oak and hawthorn Southwood and (Linnaeus) British Isles but largely predatory, hatch in April, adult Leston (1959); extremely local in the feeding on small present in late May to British Bugs south insects such as early July (2018) aphids, and the eggs and larvae of moths and beetles Miridae Calocoris Throughout the Adults mainly feed on Overwinter as eggs which Oak Southwood and quadripunctatus British Isles small insects such as hatch early in the spring, Leston (1959); (Villers) aphids and larvae of adults present May to July NatureSpot (Rhabdomiris other capsids, but (2019) striatellus/Calocoris also on young shoots striatellus) and leaves Miridae Megacoelum infusum Fairly common across At least partly, Larvae hatch mid-June to Oak Southwood and (Herrich-Schaeffer)10 Wales and England (as possibly mainly, early July, adults present Leston (1959); far north as Yorkshire) predacious on aphids, late July until early British Bugs psyllids and other October (2018) small insects, occasionally feeding on the sap from the

10 This species was found on Q. robur that were sampled in a previous Future Proofing Plant Health project (Audsley et al., 2018).

Control and management strategies for oak lace bug 23

main leaf veins and from young shoots Miridae tiliae Throughout the Largely predacious, Overwinters as eggs Almost all deciduous Southwood and (Fabricius)11 British Isles feeding on small which hatch early June to trees, especially oak, Leston (1959) insects such as early August, larvae found ash, lime and apple and until mid-September, but ladybird pupae, and most adults are present red spider mites June to mid-August Miridae Phytocoris populi Throughout the Mostly predacious on Overwinters as eggs Deciduous trees such as Southwood and (Linnaeus)12 British Isles bark lice and psyllids which hatch in spring, oak, alder and ash Leston (1959) that they find on the adults present late July trunks and twigs until October Miridae Phytocoris Throughout the Feeds on small insects Overwinters as eggs, Range of deciduous Southwood and longipennis Flor13 British Isles and mites adults found mid-July to trees especially hazel, Leston (1959); October oak and hawthorn British Bugs (2018) Miridae Phytocoris reuteri Throughout England, Mainly predatory, Overwinters as eggs Hawthorn, apple, alder, Southwood and Saunders14 also in Wales and feeds on small insects which hatch June to July, oak, elm and other Leston (1959) Scotland such as aphids, adults present early July deciduous trees psyllids and winter to late September moth larvae, and also on fruit-tree red spider mites Nabidae Himacerus apterus Found in England and Small insects such as Overwinters as eggs Deciduous trees, less Southwood and (Fabricius) Wales south of a line aphids, capsid bugs, which hatch May to June, frequently on conifers Leston (1959); from the Humber

11-13 These species were found on Q. robur that were sampled in a previous Future Proofing Plant Health project (Phytocoris were only identified to genus; Audsley et al., 2018).

Control and management strategies for oak lace bug 24

estuary to Cardigan and small caterpillars, adults present mid-July British Bugs Bay and also on mites until October (2018)

Control and management strategies for oak lace bug 25

2.6.3 Diptera: Syrphidae

There are over 280 species of hoverflies in Great Brain (NatureSpot, 2019) but only two species are associated with Quercus in the UK according to a search of the BRC Database of Insects and their Food Plants (2019): Eupeodes lapponicus (Zetterstedt) and Melangyna cincta (Fallen). Eupeodes lapponicus is considered a Nearctic species and only three records have been documented in England, near the Welsh border (NBN Atlas, 2019). Melangyna cincta on the other hand is more widely distributed across the UK being a frequent and widespread woodland species (NatureSpot, 2019); larvae have been found in association with the on beech and also on oak, sycamore and lime (NatureSpot, 2019).

2.6.4 Hymenoptera

There has only been one report of a associated with oak lace bug: a previously unknown belonging to the Erythmelus genus (named Erythmelus klopomor) has been observed emerging from oak lace bug eggs on Q. macrocarpa in Missouri, USA (Triapitsyn et al., 2007), and is also known to attack the avocado lace bug Pseudacysta perseae (Heidemann) (Peña et al., 2009). A search of the Universal Chalcidoidea Database (Noyes, 2018) indicates that there are three species of Erythmelus known to occur in the UK: E. panis (Enock), recorded in England, is known to be associated with Tingidae (including C. ciliata) elsewhere in its distribution range; E. rex (Girault), recorded in Wales, is also associated with Tingidae in its distribution range but would appear to be associated with herbaceous plants; E. flavovarius (Walker, 1846) is recorded as present in England but there are no known associations with Tingidae elsewhere in its distribution range. Information regarding the plants that these are associated with appears to be sparse. For instance, E. panis is reported as associated with C. ciliata but Platanus spp. are not recorded as plant associates for the parasitoid whilst two of the known hosts for C. arcuata namely, Malus sylvestris and Prunus avium are.

Sheeley and Yonke (1977) did not find any evidence of parasitism in the seven species of lace bug that they studied but the study did not include C. arcuata. There are reports of one species of parasitoid, Anagrus takeyanus (Hymenoptera: Mymaridae), attacking eggs of the andromeda lace bug (Stephanitis takeyai Drake and Maa; Gordh and Dunbar, 1977) and the azalea lace bug (Stephanitis pyrioides (Scott); Balsdon et al., 1996) in the USA; it is thought that this parasitoid is not native to the USA but rather was introduced along with S. takeyai from Japan in the 1940s (Gordh and Dunbar, 1977). Puttler and Triapitsyn (2006) also report that a new species of Anagrus (named A. virginiae) has been reared from eggs of the chrysanthemum lace bug (C. marmorata (Uhler)). There are currently 104 confirmed mymarid species in Britain and Ireland and this includes eleven species in the genus Anagrus (Dale-Skey et al., 2016) that parasitise leaf/ eggs: A. atomus (Linnaeus); A. avalae Soyka; A. bakkendorfi Soyka; A. breviphragma Soyka; A. ensifer Debauche; A. fennicus Soyka; A. incarnatus Haliday; A. nigriceps (Smits van Burgst); A. obscurus Förster; A. subfuscus Förster and A. ustulatus Haliday. However, none of these species appear to be associated with oak.

2.6.5 Araneae

The spider Achaearanea lunata (Clerck) (Theridiidae) is listed as a natural enemy of C. ciliata (CABI, 2018). It is known to be widespread throughout much of England south of the Humber but absent in

Control and management strategies for oak lace bug 26

the west and is generally uncommon; it is associated with dense and shaded woodland sites and found on the branches of trees 1.5 – 2 m above the ground and on the trunks (e.g. of old trees) (British Arachnological Society, 2019).

A presentation by Franjević et al. entitled “Oak lace bug Corythucha arcuata (Say, 1832) (Heteroptera: Tingidae) in Croatia; insights, protection strategies and novel survey methods” given at the Forest Protection Expert Colloquium (2018; slides only available) would suggest that yellow sac spiders, crab spiders and false spiders are either implicated as a natural enemy for oak lace bug in Croatia or that they are currently under investigation for potential biocontrol strategies.

Yellow sac spiders (Cheiracanthium spp.) are reported to be beneficial predators of agricultural fields however, they are also mildly venomous to humans (Wikipedia, 2019). Three species (C. erraticum (Walckenaer), C. pennyi O.P. Cambridge and C. virescens (Sunevall) are present in Britain (Merrett et al., 2014) but none are associated with woodlands or deciduous tree species (British Arachnological Society, 2019). Philodromus species (crab spiders) also have potential as biocontrol agents for example in pome fruit orchards (Michalko and Pekar, 2015). Eleven species of Philodromus are recorded as present in Great Britain (Merrett et al., 2014) and Table 3 lists those associated with woodland habitats/trees. Only two species of false crab spiders (Thanatus spp.) are recorded as present in the Great Britain (Merrett et al., 2014) but none are associated with trees and wooded areas (British Arachnological Society, 2019).

Table 3. Species of crab spiders (Philodromus spp.) recorded in Great Britain and associated with wooded areas and/or broad-leaved trees. Information taken from Merrett et al. (2014) and the British Arachnological Society (2019).

Species Habitat Distribution in Great Time of year found Britain Philodromus Wooded habitats within the Widespread in Adults mainly found in dispar herbage, lower branches of trees southern Britain early summer Walckenaer and shrubs, overwinters in leaf litter Philodromus Wooded habitats, thickets, Widespread but Adults found early to aureolus (Clerck) hedgerows and scrub usually in more scattered in mid-summer bushes and lower branches and north and west usually on older trees, probably overwinters in leaf litter Philodromus Mature oak trees in open Widespread in south Adults found late May praedatus O.P. situations, wood pasture, edge of east England but few to end of June Cambridge woodlands and old hedgerows records elsewhere in the country Philodromus More usually associated with Widespread in Adults found early to cespitum scrub and herbage but sometimes lowland southern mid-summer (Walckenaer) found on trees in heathland, Britain but scattered heathery bogs, hedgerows, scrub in the north and wooded habitats Philodromus Lower branches and trunks of old Rare, widely Adults found mid-May longipalpis Simon oak trees in open situations, scattered sites in to mid-July southern England

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juveniles found in heather under open oak woodland Philodromus Mainly found on pine, yew and Uncommon, Adults found May to collinus C.L. Koch Douglas fir branches but has been southern and July found on broadleaved trees in eastern England as mixed woodland and coniferised far as Yorkshire ancient woodland Philodromus Broad-leaved or mixed woodland Southern half of Adults found May to albidus on the lower branches of broad- England July Kulczyński leaved trees, such as oak, at the edges of clearings and rides, also in old hedgerows and green lanes Philodromus Found on the trunks of pine and Scattered localities in Adults found May to margaritatus broad-leaved trees especially the south of England; June (Clerck) when they are covered in lichen UK Biodiversity Action Plan species

Control and management strategies for oak lace bug 28

Chapter 3. Oak lace bug in Europe

In Italy, oak lace bug was first observed in a park near the city of Milan in the spring of 2000 (Bernardinelli and Zandigiacomo, 2000), and it has been suggested that it was introduced through the importation and planting of infested trees (Anderson, 2018). Surveys conducted during the autumn of 2000 through to the end of February 2001 indicated that it was present at a number of sites in a 7000 km2 area across the Lombardy and Piedmont region (Bernardinelli, 2000). Evidence suggests that the insect must have been established in the area for some time, and possibly dispersing along roads, and that any attempt to stop it from spreading further would be futile (Bernardinelli and Zandigiacomo, 2000; Bernardinelli, 2000). In Italy, despite its presence for 18 years, no significant damage from oak lace bug attack is recorded (reported within Anderson (2018)) and the insect is not considered to be a major pest (Csóka et al., 2013).

Following the initial recording of oak lace bug in Turkey in 2002, when it had a limited distribution in the province of Bolu (Mutun, 2003), it spread to a further eight neighbouring provinces during the following four years totalling an area of 28,116 km2 (Mutun et al., 2009). Similar degrees of spread covering distances of over 200 km in only a few years have been reported in Russia (250-270 km in less than two years covering an area of more than 19,000 km2; Neimorovets et al., 2017), Bulgaria (Simov et al., 2018) and Hungary (Csepelényi et al., 2017b).

Oak lace bug was first detected in Switzerland (2002) when it was intercepted in combination flight traps (passive window trap and yellow shell) that had been installed in a clearing as part of a biodiversity study of invertebrates (Forster et al., 2005). The following year more individuals were intercepted in the same type of trap this time located on freshly deforested areas. Forster et al. (2005), reporting on the first observation of oak lace bug in Switzerland, suggest that the spread of oak lace bug cannot be stopped, and that control measures are difficult to carry out and are not justified. They suggest that at best, prematurely fallen foliage on which there may still be larvae can be collected and destroyed.

Alim’agri (2017), reporting on the first record in France, suggests that the yellowing of leaves in the summer and premature leaf fall will be an aesthetic problem in parks and gardens but damage to infested oaks is likely to be minimal.

In contrast, there is now increasing evidence from Croatia and Hungary (Csóka et al., 2013; 2017; Csepelényi et al., 2017b; Pernek and Lacković, 2017; Berta et al., 2018; Franjević et al., 2018) that oak lace bug is going to become an increasingly important pest in European oak forests and that the levels of damage that this insect causes will increase in southern Europe, especially in places where it can complete more than two generations per year.

3.1 The situation in the Republic of Croatia

The presence of oak lace bug was confirmed within five locations in the Spačva Basin, Croatia in 2013, predominantly on pedunculate oak but also on U. minor (field elm), European crab apple and blackberry (to a lesser extent), all of which were suffering from a yellowing of the leaves (Hrašovec et al., 2013).

From the initial findings in 2013, the pest has spread very rapidly within Croatia (Berta et al., 2018). In 2015, monitoring of spread and intensity of attack by MODIS satellite - Normalised Difference

Control and management strategies for oak lace bug 29

Vegetation Index15 (MODIS-NDVI) revealed that 37,000 hectares of the Spačva Basin was affected, with high intensity attack occurring in the central part of the basin (Berta et al., 2018). In 2016, 57,000 hectares of the Spačva Basin was affected, and intensity of attack was reported at 60-80% across the whole area (Berta et al., 2018). The following year (2017), levels of intensity reached 100%, over 99% of the Spačva Basin forest (an area totalling approximately 60,000 hectares) with an additional 50,000 hectares of forested area in other parts of Croatia also under attack (Berta et al., 2018). However, this form of satellite imagery cannot detect lower intensity attack (20-40%; Berta et al., 2018). Results of the 2017/2018 mapping indicate that the spread of oak lace bug is following the main road networks within Croatia (Berta et al., 2018). Rapid spread within Hungary has also been attributed to hitchhiking along roads along with mild winters, hot dry summers and a lack of natural enemies (Csóka et al., 2017). In Croatia, leaf damage starts to occur in late April as the adults feed; damage becomes observable towards the end of May coinciding with the hatching and feeding of the first generation larvae, and by the end of June more than 60% of the leaf surfaces are damaged by feeding of the pest (Franjević et al., 2019).

Many (approximately 76%) of the state-owned forests within Croatia are managed by the state-owned company Hrvatske šume Ltd. and are FSC certified (Franjević et al., 2019). This certification prohibits the use of many of the more effective active ingredients due to their hazardous properties; protection against invasive species such as oak lace bug and sustainable forest management is therefore challenging under the current situation (Franjević et al., 2019). Research into potential control methods under such circumstances appears to be underway with the Croatian Ministry of Agriculture funded project “The Study about effectiveness of measures for prevention of spreading of the oak lace bug”16 but results of this study do not appear to be in the public domain. However, one published article briefly describes some research on the use of protective cardboard rings, glue, and protective netting (Storanet®) around the trunk, NeemAzal TS (a natural broad-spectrum insecticide containing the active ingredient azadirachtin obtained from the fruit and seeds of Azadirachta indica), ASSET (a non-synthetic contact insecticide containing the active ingredient pyrethrin derived from Chrysanthemum cinerariifolium), and trunk injection of KRAFT 18 EC (active ingredient abamectin) using the Blade for Infusion in Trees (BITE®) injection system (Franjević et al., 2019). However, ASSET and NeemAzal TS (both applied as aerial spray application) are reported as ineffective although failure of NeemAzal TS was attributed to application during a period when egg masses, which are not affected by NeemAzal TS, were present (Franjević et al., 2019). These authors do not provide any results on the use of the protective carboard, netting or caterpillar glue however, they do report that treatment with abamectin using BITE® application resulted in partial protection from oak lace bug.

In June 2017, the Republic of Croatia Ministry of Agriculture issued the “Order to take measures to prevent the spread of the harmful organism Corythucha arcuata (Say, 1832) – oak lace bug” (RoC Ministry of Agriculture NN 52/2017 (1195)) prescribing measures to be taken to prevent the spread of oak lace bug (Article 1) for the “protection of the public interest and preserving the forests of native

15 Normalized Difference Vegetation Index (NDVI) is a standardised way to measure healthy vegetation by measuring the difference between near-infrared (which vegetation strongly reflects) and red light (which vegetation absorbs). Healthy vegetation reflects more near-infrared and green light but absorbs more red and blue. Values range from -1 to +1 with a higher value indicating healthier vegetation. https://gisgeography.com/ndvi-normalized-difference-vegetation-index/. Accessed 3rd March 2019.

16 https://oikon.hr/the-study-about-effectiveness-of-measures-for-prevention-of-spreading-of-the-oak-lace- bug/.

Control and management strategies for oak lace bug 30

oak species in the continental territory of the Republic of Croatia, as a domain of interest for the Republic of Croatia, or preventing further damage” (Article 2). Article 3, paragraph 1 lists the main host plants as Q. robur and Q. petraea while paragraph 2 lists other hosts within the meaning of the Order (Q. cerris, Q. pubescens, Q. rubra, as well as C. sativa, M. sylvestris and European hornbeam (C. betulus). Article 4 identifies the areas that are considered infected, endangered or of special importance for monitoring and Article 5 states that owners are required to monitor the health of the plants that they grow, and produce, and to immediately inform forest inspectors if oak lace bug is found.

Article 6 of the Order concerns the transportation of wood:

• Paragraph 1: Temporarily limits for a period of two years, the transport of wood that completely or partially retains its natural surface area (i.e. with and without bark), or planting material of the species listed under Article 3; • Paragraph 2: Transport can be carried out exclusively from the place of production to the place of processing (cutting and production) and of the shortest distance possible; • Paragraph 3: Wood must be processed to lose its original shape and dried to below 20% moisture content before placing on, and transporting to, the market; • Paragraph 4: Waste from the processing referred to in 6(3) e.g. bark, wood chips, saw dust can only be transported in lorries that have a covered cargo area; • Paragraph 5: Plant material referred to under Article 3(paragraph 1) may only be moved and used within a single seed zone; • Paragraph 6: Owners and holders at places of production of planting material of the species listed in Article 3 (paragraph 1) will be obliged to restrict access to areas suspected of being infected, or where the presence of oak lace bug is confirmed, and to implement any measures prescribed by a forest inspector.

Article 7 states that owners will bear the cost of implementing any measures prescribed by the Order. Article 8 states that the Forestry inspectorate and the Ministry will jointly conduct supervision of measures prescribed by the Order and finally, Article 9 states that a forest inspector may order the return of a planting consignment to the place of production, or wood to the processing site, in the Republic of Croatia if oak lace bug is found, and to determine measures necessary to prevent spread.

However, on the 15th May 2018, this Order was amended to ease restrictions on transportation of wood and wood products without bark (Republic of Croatia Ministry of Agriculture NN 49/2018 (975)). In the amended Order, the previously defined restrictions of Article 6 paragraph 1 only apply to wood retaining its natural round surface with bark, and planting material of the species referred to in Article 3 paragraph 1 i.e. Q. robur and Q. petraea (Republic of Croatia Ministry of Agriculture NN 49/2018 (975)). Additionally, the original paragraphs 3 and 4 of Article 6 were deleted in the amended Order i.e. wood no longer needs to be processed to lose its original shape and dried to below 20% moisture content before placing on, and transporting to, the market, and waste from such processing no longer needs to be transported in lorries with a covered cargo area (Republic of Croatia Ministry of Agriculture NN 49/2018 (975)).

Croatia communicated their national measures against oak lace bug and the movement of oak logs, along with the results of a study evaluating the efficacy of these measures to limit the spread of oak lace bug at the European Commission Standing Committee on Plants, , Food and Feed (SCOPAFF) meeting held in Brussels 11-12th October 2018. The details of this communication do not appear to be published however, Anderson (2018) indicates that the Croatian authorities reported

Control and management strategies for oak lace bug 31

that adoption of the Croatian Order was slowing the spread of oak lace bug. The published summary report from the SCOPAFF meeting17 states that an exchange of views occurred and that “concerns were expressed about the efficacy of the measures to allow a real eradication or at least containment”. The summary report also indicates that “some of the other affected Member States would not support emergency measures”. The Commission requested “Croatia to withdraw the national decree that is limiting movement and trade of oak logs” and stated an official letter would be sent to the competent authority.

3.2 Implications for the UK

Currently, statutory action is required against interceptions of oak lace bug (Defra, UK Plant Health Risk Register). There is now greater evidence from Europe as to the potential impact of oak lace bug, and the strain that may result to trees and ecosystems, albeit still with many uncertainties (Anderson, 2018). More evidence is also now available with regard to the roles that anthropogenic activity may play in contributing to the spread of the insect. This evidence has prompted a number of actions from the UK government Department for Environment Food and Rural Affairs (Defra):

• An update (Anderson, 2018) to the 2007 pest risk analysis for Corythucha arcuata; • The release of a pest alert (oak lace bug is also a priority pest for Observatree thus raising awareness of the pest with the public through citizen science); • Seeking permission for the implementation of a Protected Zone (Defra Plant Health Portal; Appleby, 2018).

Details of the UK Rapid Pest Risk Analysis (Anderson, 2018) for C. arcuata are summarised in the following paragraphs.

3.2.1 Risk

The two native oaks (Q. robur and Q. petraea) are widespread in the UK, and therefore the whole of the UK can be considered an endangered area from oak lace bug attack, but there is currently not enough information available to assess whether other host species would be endangered by attack from this insect (Anderson, 2018).

Risk of entry into the UK has been raised, based on the new evidence, and also takes into account that whilst oak trees are the preferred host for C. arcuata, a number of other trees are potential hosts. The three routes of entry are identified as (Anderson, 2018):

1. Plants for planting (likely with low confidence)

Quercus plants with leaves are not allowed to be imported from non-European countries reducing the likelihood of introducing eggs into the UK from North America. However, overwintering adults (under crevices in the bark of trunks and large branches) have the potential to be present on dormant plants coming from all infected areas of the world and would most likely be associated with plants for planting. That said, most trees imported into the UK for planting are young and therefore do not have many bark crevices for the adults to

17 https://ec.europa.eu/food/sites/food/files/plant/docs/sc_plant-health_20181011_sum.pdf (paragraph A.08; accessed 13th February 2019).

Control and management strategies for oak lace bug 32

hide in. However, young trees are often moved around Europe before being sold as part of industry practice; they may be moved down to Italy for a couple of years to aid growth, and then returned to more northern countries such as and the Netherlands for a year of ‘finishing’ before being sold. To date, oak lace bug has not been found in northern European countries.

Fewer large trees are imported but in contrast are deemed to present a significant risk because it would be difficult to ascertain whether they are free of the pest, and also because these larger trees are more likely to be transported straight to planting sites. With the exception of Q. suber, oak trees with a girth ≥ 8cm at a height of 1.2 m above the root collar are currently required to be inspected in relation to oak processionary moth (Thaumetopoea processionea L.) and this may help to reduce the likelihood of importing oak lace bug on oak trees (but not on other potential host plants that do not have a requirement for inspection).

2. Wood and wood products with bark (likely with medium confidence)

Products such as logs, wood with bark still associated, and wood chips that include bark from any species considered to be an overwintering host of oak lace bug could represent a pathway of entry into the UK. Wood without bark was not included in the risk analysis. The quantities and frequencies of wood and wood products of concern from countries where oak lace bug is present is unclear, largely due to the uncertainties surrounding the overwintering hosts. In a study reported by Csepelényi et al. (2017a), 97% of overwintering adults (from a total number of 4770 individuals) were found on oak but overwintering adults were also found under the bark of elm, elder, poplar, ash, chestnut and maple. A much greater volume of oak timber in the rough (with some residual bark likely) is thought to be imported into the UK from infected countries compared to oak firewood but numbers relating to firewood are thought to be an underestimate.

3. Hitchhiking on transport (moderately likely with low confidence)

The nearest outbreak site (southern France) is some distance away from the UK and the sea crossing acts as a barrier. The Rapid PRA (Anderson, 2018) does however suggest that hitchhiking as an entry pathway is likely to be a cause of increased concern as the pest moves across Europe.

The Rapid PRA (Anderson, 2018) deems, with high confidence, that oak lace bug would be likely to establish in the UK if it arrived. The fact that the native range of the pest includes many northern and eastern states of the USA and southern Canada would suggest that the temperate climate of the UK is not likely to hinder establishment. It is thought that the insect would more likely follow the lifecycle observed in the USA with two complete generations per year and a partial third rather than the three generations and partial fourth that has been observed in southern Europe. The pest is also likely to be able to overwinter in the UK. One study has indicated a mortality rate of 36.5% during a relatively cold winter in Hungary (i.e. nearly two thirds of the population survived the cold conditions; Csepelényi et al., 2017a) however, alpine winter conditions are hypothesised to be the limiting factor in oak lace bug populations in the Cantone Ticino, and Valtellina and Alto Lario regions of Switzerland and Italy (Lombardy), respectively (Dioli et al., 2007) with the authors suggesting that the adults would not have as many suitable winter shelters.

Control and management strategies for oak lace bug 33

The natural rate of spread is considered to be slow. However, contrary to earlier thoughts, and based upon more recent information from southern Europe (as detailed earlier in this chapter), it is thought that the pest can spread quickly with trade and transport (with medium confidence applied to this rating). The Rapid PRA (Anderson, 2018) does suggest that it is not clear what proportion of the spread observed in Croatia is down to the movement of logs, timber and woodchips or natural spread assisted by the movement of road traffic.

Impacts within its existing distribution are rated as medium, with a medium level of confidence (Anderson, 2018) for the reasons discussed earlier in this chapter. However, in the UK pest risk analysis area, the greatest uncertainties surrounding oak lace bug are in relation to the potential impacts (Anderson, 2018). Economic impacts are considered to be small with medium confidence: it is thought populations in the nursery trade are more likely to be controlled and impacts on wood production would not be as high as in areas of Europe where it is already established (Anderson, 2018). Environmental impacts are rated as medium but there is low confidence in this rating due to the speculative nature of cumulative and long-term impacts (e.g. effects on seedlings and young stands, acorn crops, effects on the species that rely on oak for habitat and food) (Anderson, 2018). The risks presented by alien species to forestry are usually very high because of the difficulties associated with implementing eradication strategies and carrying out control treatments (Bernardinelli, 2007); the chances of eradicating oak lace bug from a forest environment are small and the pest will likely exert cumulative effects on the health of amenity trees and woodlands (Anderson, 2018). Environmental impacts are likely to be determined by the rate at which populations increase (and spread) and the levels that they reach, which in turn will be determined by climate and presence of natural predators. A temperate climate might prevent oak lace bug from attaining the levels seen in southern Europe whilst the lack of natural predators and parasitoids may mean that oak lace bug would attain higher levels in the UK than seen in its native North America. That said, there is also the possibility of impacts in the UK during a hot summer when trees will be more stressed, and there is concern that oak lace bug could become another contributing factor in oak decline especially in areas of the UK where trees are already under threat from other invasive pests. Social impacts are rated as medium, and with medium confidence, on the basis that oak is an iconic tree in the UK and hence the public will likely express concern over any pests of oak (Anderson, 2018).

3.2.2 Risk management options

Whether or not this insect could be eradicated or contained if it were to arrive in the UK would be dependent on the circumstances of the outbreak. An effective chemical treatment may be possible if an outbreak were to be discovered at a nursery, or on a small number of trees close to a wood importer for instance, soon after import (Anderson, 2018). Such an eradication, using bifenthrin, has been achieved when the related sycamore lace bug was detected in the UK in 2006.

However, if the insect is found in the wider environment, an oak forest for instance, then it is less likely that eradication would be achieved due to the potential number of hosts that would be present in such an environment and the difficulties in treating large trees covering large areas (Anderson, 2018). There are no biological control options currently available for managing this pest and FSC restrictions on the use of highly effective chemical controls also further reduce the chances of successful eradication or containment in the wider environment.

Control and management strategies for oak lace bug 34

Removal and destruction of infested trees is unlikely to be an effective means of eradication or containment due to the potential range of hosts and the materials that oak lace bug could be present on (e.g. living wood/dead wood/leaf litter); indeed, it is considered that this option may be more destructive than the pest itself (Anderson, 2018). Sancisi-Frey (2017) consider that it is very important not to remove leaf litter, soil, wood or foliage from infested sites because lace bugs could be present in all these media.

Risk management options should therefore centre around ensuring that the insect either does not enter the UK or if it does that it is detected very quickly after arrival. The first option (exclusion) requires the implementation of a Protected Zone (Anderson, 2018), and this is something that Defra is currently seeking (Appleby, 2018; Defra Plant Health Portal).

Implementation of a Protected Zone would mean one of the following possible requirements for the import of plants for planting (Anderson, 2018):

1. To have been grown through their entire life in places of production in countries where oak lace bug is not known to occur; 2. To have been grown through their entire life in an area free from oak lace bug established by the national plant protection organisation in accordance with relevant International Standards for Phytosanitary Measures; 3. Produced in nurseries which, along with the surrounding area, have been found free of oak lace bug on the basis of official inspections and surveys conducted at appropriate times; 4. To have been grown through their entire life in a site with complete physical protection against the introduction of oak lace bug and to have been inspected at appropriate times and declared free of the pest.

One of the following possible requirements would be needed for oak wood (Anderson, 2018):

1. Wood should be bark free; 2. Wood should carry an official statement confirming that it has either originated from an area known to be free of oak lace bug or that it has undergone kiln-drying to achieve < 20% moisture content (expressed as a percentage dry matter) using an appropriate time and temperature schedule (NB. there is no actual evidence of the effect that kiln drying has on oak lace bug).

Bernardinelli (2007) is also in agreement that careful control of goods coming from abroad would be a decisive action to take to protect forestry from the risks associated with harmful alien species.

Early detection has a greater chance of occurring if people are aware of the dangers of this pest and are on the lookout for it. Bernardinelli (2007) suggests that constant monitoring of forested areas by trained personnel is a reasonable action to take to help protect against the dangers of invasive species. To this end, Defra issued a pest alert for oak lace bug in August 2018 to alert nursery and forestry industries (Defra, 2018). Oak lace bug is also a priority pest for Observatree thus raising awareness of the pest with the public through citizen science.

If found in the UK, restrictions on the movement of planting material and wood products with bark could be put in place in an effort to contain the pest, as has been done in the Republic of Croatia, although it is uncertain how much of the spread observed in southern Europe is down to road and rail travel in general rather than specifically the transport of these commodities (Anderson, 2018).

Control and management strategies for oak lace bug 35

Chapter 4. Uncertainties identified in the literature that would benefit from further research

A number of uncertainties surrounding oak lace bug have been identified in the literature (Csóka et al., 2017; Anderson, 2018) and gaps where further research is required to provide a better understanding and solutions to the problems surrounding spread and control:

1. Are the Italian and Turkish introductions of oak lace bug independent of each other (Csóka et al., 2017)?

2. The current most northern record of oak lace bug is in Felsőtárkány, north Hungary (Csepelényi et al., 2017b) and the current most westerly record is in southern France (Alim’agri, 2017; Anderson, 2018). Csóka et al. (2017) ask whether climate will restrict spread to the North and West of Europe?

3. What are the direct and indirect impacts of long-term damage on oak tree growth and health (Csóka et al., 2017; Anderson, 2018)?

4. What are the impacts on oak seedlings and young stands (Csóka et al., 2017; Anderson, 2018)?

5. What are the impacts on the acorn crop (Csóka et al., 2017; Anderson, 2018)?

6. Can oak lace bug act as a vector for pathogens of oak (Csóka et al., 2017)?

7. Will C. arcuata and C. ciliata hybridise (Csóka et al., 2017)?

8. How much damage should be expected, and how serious will the damage be (Csóka et al., 2017)? In particular, the potential impact of oak lace bug in the UK is uncertain as it is possible that due to our temperate climate, populations may not achieve the same levels in the UK as observed in southern Europe where it is warmer (Anderson, 2018); the UK climate is similar to the climate in some areas of North America where oak lace bug is native and not a pest however, the UK lacks the native predators that keep the North American populations in check.

9. What is the relative importance of the different host species; for instance, are other hosts only utilised when population levels become high, and how dominant a host are Quercus in comparison to other hosts. (Anderson, 2018)?

10. What can be done to reduce the impact of oak lace bug (Csóka et al., 2017)?

11. Can higher resolution multispectral satellite imagery (e.g. LANDSAT 8/SENTINEL 2) improve remote monitoring of oak lace bug attack (Berta et al., 2018)?

Control and management strategies for oak lace bug 36

Conclusions

There is now growing concern, given the situation in the Republic of Croatia, that oak lace bug has the potential to become a serious primary pest of oak in favourable environments, with severe attack and rapid spread causing considerable amounts of damage not only to the infested plants themselves but also to the wider ecosystem. However, there is much uncertainty surrounding the impact that oak lace bug could have in the UK if it were to be introduced and become established in the UK. It is highly likely that this insect will be able to establish in the UK and would have the potential to become widespread given the widespread distribution of pedunculate and sessile oak. However, it is possible that the more temperate climatic conditions of the UK will mean that the oak lace bug follows the typical life-cycle observed in North America of two generations and a partial third per year rather than three generations and a partial fourth observed in the warmer regions of southern Europe. That said, natural enemies in North America also help to keep populations of this insect in check, minimising the damage that it inflicts, but since it is not known whether any predatory species native to the UK would predate on oak lace bug, a similar outcome cannot be guaranteed in the UK.

Oak lace bug primarily feeds on species of oak however, there are many other host plants that it is known to be associated with including some species of Castanea, Prunus, Malus, Rosa, Rubus, Ulmus, Acer, and Tilia. At present the relative importance of these other species is not known for instance, are these other species only utilised when oak becomes limiting?

Dispersal of oak lace bug within Europe has mostly been linked to anthropogenic activity, especially hitchhiking on transport (both road and rail). This is often associated with the movement of oak logs/timber from forested areas although it is unclear how much of this is due to the presence of the insect on the logs/timber itself and how much is due to hitchhiking on the vehicles transporting these commodities.

Eradication of the insect, should it be introduced into the UK, is unlikely if it is found in the wider environment but may be possible with a quick and decisive response if it is found e.g. at a nursery or on a small number of trees in close vicinity to e.g. a wood importer shortly after import. Containment and management options should therefore be given consideration. It is considered that destruction and removal of host plants would not be a viable option, given the number of host plants that the insect is associated with, and that it can overwinter off host at ground level, and is thought to be potentially more damaging to the local environment than the insect itself. Management options will be dependent on the environment in which the insect is found (e.g. forest, open parkland, urban). A range of insecticides are reported in the literature for the control of lace bugs and these may be a suitable control option in some environments with appropriate application methods. However, issues with application often mean that either efficacy is poor or that certain active ingredients cannot be used. For instance, it is often not feasible to use spray applications (which must be directed at the underside of the leaves where the insect feeds) in forested areas, and many of the effective ingredients are classed as highly hazardous chemicals by the Forest Stewardship Council and therefore prohibited from use in areas under FSC management. There are currently no biological control options for oak lace bug, and only limited research has been undertaken into such control measures. Control measures should concentrate on reducing the population of the first (overwintering) generation of oak lace bug and the eggs/larvae produced by this generation due to the exponential increase of generations throughout the season.

Control and management strategies for oak lace bug 37

Recommendations

It must be noted that this document is a literature review, and as such the information contained within it is gathered from scientific publications, grey literature and information available on the internet rather than from any practical experience on the biology, control and management of oak lace bug.

There seems little doubt that if oak lace bug should arrive and establish in the UK, eradication is unlikely because of its ability to have several overlapping generations per year, multiple host plants and a lack of suitable and effective control measures. Every effort should therefore be made to prevent this pest from entering the UK in the first place.

It is our understanding that a two-year Euphresco project linking with other Europeans who have an interest in collaborating on oak lace bug is under consideration. At the time of writing this review, the full research activities of this project have not been defined but it is likely to include a “Management” work package which will include control options (pers. comm. David Williams, Forest Research, UK).

Following review of the literature, the authors would recommend consideration of the following actions:

1. Liaise with the relevant national regulatory authorities and research personnel from countries where oak is under intense attack by oak lace bug to keep up to date with advances in their control and management strategies. 2. To have a robust contingency plan and management strategy in place to deal with any potential outbreak as soon as the relevant authorities have been alerted to the possibility of such an outbreak. Strategies will differ in accordance with the circumstances of the outbreak; eradication using effective chemicals is only likely to be possible under exceptional circumstances such as if an outbreak were to be discovered at a nursery, or on a small number of trees close to a wood importer for instance, soon after import (Anderson, 2018) therefore it is important to be able to act quickly and decisively in such a situation. 3. Consider trapping at strategic locations e.g. at ports where oak is imported into the UK/wood storage facilities to maximise the chances of early detection. Whilst there are no pheromone traps currently available for oak lace bug (no pheromones have to date been identified for C. arcuata), Chireceanu et al. (2017) report the use of yellow sticky traps to capture adults in a field survey for early detection and Forster et al. (2005) report that oak lace bug was first detected in Switzerland when it was intercepted in combination flight traps (passive window trap and yellow shell). 4. There is a great deal of uncertainty surrounding the likely impact of oak lace bug in the UK should it establish. It would be helpful to ascertain, e.g. by modelling, the probable number of generations per year that this insect is likely to have in the UK as this will influence the impact. 5. Obtain specific data on overwintering hosts in order to establish whether it is likely that this insect could come into the UK on wood/logs other than oak. 6. Control aimed at the overwintering adults/first generation is likely to be more effective at reducing the impact of this insect because intensity of attack increases with the exponential increase in numbers from each generation through the year. Research should therefore focus on controlling these stages. 7. The efficacy of currently available insecticide products containing pyrethroid, chitin synthesis inhibitor and neonicotinoid active ingredients should be established along with suitable

Control and management strategies for oak lace bug 38

application methods. The efficacy of plant essential oils as a means of controlling oak lace bug could also be investigated. 8. There are currently no biological control options available for oak lace bug, with only limited research reported for the potential use of entomopathogenic fungi. Further research into the potential use of entomopathogenic fungi, and also entomopathogenic nematodes, would be beneficial. 9. From the literature, it appears that there are species of predatory bugs, lacewings, syrphids and spiders that inhabit oak trees and have the potential to predate on oak lace bug. It may be useful to conduct a survey of predatory species present on oak in the UK and to establish the prey preferences of the more common predators (e.g. laboratory trials to establish whether they will predate on oak lace bug eggs). It is also important to consider the life cycles of these predatory species to establish compatibility with the oak lace bug life cycle. Similarly, further information on the Erythmelus species of parasitoid present in the UK, particularly E. panis, could be obtained to establish whether they are capable of parasitising oak lace bug eggs and to ascertain their habitat preferences.

Control and management strategies for oak lace bug 39

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