A Defra Network partnership delivering interdisciplinary plant health FUTURE PROOFING research to improve biosecurity and build capability Plant Health Task 5.6. Control of Corythucha arcuata Evaluating the Control and Management Options for Oak Lace Bug (Corythucha arcuata) 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 Europe …………………………………………………………………………………………………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) (Hemiptera: Tingidae) 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 Tilia. Oak lace bug is native to North America where it is not generally considered to be a pest 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 (Italy) 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. Hungary and the Republic of Croatia report rapid spread of the insect, 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 insecticides 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, Corythucha ciliata (Say) the sycamore lace bug (the name ‘Platanus’ 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); Switzerland (2002/3; Forster et al., 2005); Bulgaria (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); Romania (2015; Chireceanu et al., 2017); Russia (2015; Neimorovets et al., 2017); Slovenia (2016; Jurc and Jurc, 2017); Albania (2016; Csepelényi et al., 2017b; Berta et al., 2018); France (2017; Alim’agri, 2017); Bosnia-Herzegovina (2017; Dautbašić et al., 2018), and most recently in Slovakia (2018; Zúbrik et al., 2018) and Greece (2018; Pernek and Lacković, 2017; Anderson, 2018). Csóka et al. (2017) indicate that the rate of spread across south eastern Europe 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 instar (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.