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Task 5.4.4 Collect baseline data on native in

A review of natural levels in oak in Great Britain

Rachel Down, Damian De Marzo, Chris Malumphy and Neil Audsley (Fera)

31st March 2019

Work Package 5 Control

Contents

Abstract …………………………………………………………………………………………………………………………………………. 3

Chapter 1. Introduction …………………………………………………………………………………………………………………. 4

Chapter 2. Cynipid oak galls of Great Britain …………………………………………………………………………….…… 6

Chapter 3. Interactions between oak galls, their associated communities and Torymus sinensis ….. 87

Summary ……………………………………………………………………………………………………………………………………. 104

References ……………………………………………………………………………………………………………………………….… 105

Parasitism levels in oak galls 2

Abstract

Oak gall (: Cynipidae) are typically characterised by their complex life-cycles, alternating between sexual and asexual generations. The galls that they induce are both and generation specific and show an astonishing degree of diversity and complexity. Oak galls also support a very rich and diverse, well-structured, community of parasitoids and cynipid (Hymenoptera: Cynipidae, tribe Synergini). The majority of parasitoids associated with cynipid oak galls belong to the hymenopteran super-family Chalcidoidea, and are distributed across six families: , , , , and . species live within the cynipid galls but do not themselves induce primary gall formation. They are classified as lethal and non-lethal according to whether or not their chambers encroach upon those of the gall inducer thus killing the gall inside. Relationships within the galls are complex: parasitoids can attack the larvae, inquiline species, and other species (known as hyperparasitism) present within the gall. Parasitoid species are rarely host specific and will usually attack many different species of gall wasp. However, the sexual and asexual generation galls usually support different species of parasitoids although it is often the case that the same generation of closely related gall wasps will support similar communities of parasitoids and inquilines. There are approximately 200 species of cynipid gall wasps, and 100 species of chalcid parasitoids and 38 species of inquilines recorded as associated with them across the western Palaearctic region.

This review aims to provide life-cycle details, and levels of attack for associated parasitoids and inquilines for oak gall wasp species known to be present in Great Britain. This information is being gathered prior to the potential release of a non-native biocontrol agent, the chalcid parasitoid Torymus sinensis Kamijo (Hymenoptera: Torymidae), for control of the invasive Oriental gall wasp kuriphilus Yasumatsu (Hymenoptera: Cynipidae), a species of gall wasp that attacks sweet chestnut trees (Castanea spp.). Concern has been raised that this potential biocontrol agent may be able to utilise native and naturalised oak gall wasps in Great Britain as an alternative host. Indeed, this has been observed in other areas of Europe (Italy) where T. sinensis has already been released. Obtaining baseline data on natural parasitism levels in oak galls prior to release will allow for effective monitoring of competition between T. sinensis and native parastoid species should T. sinensis be released into the environment.

Parasitism levels in oak galls 3

Chapter 1. Introduction

The Oriental or Asian chestnut gall wasp, Yasumatsu (Hymenoptera: Cynipidae), is a species that attacks sweet chestnut trees (Castanea spp.). It is native to China but has been accidentally introduced into other geographical regions including Japan (Moriya et al., 2003), the USA (Payne et al., 1975), and western Europe in 2002 when it was discovered in Italy (Brussino et al., 2002). Since its discovery in Italy it has spread into numerous western European countries (Down and Audsely, 2016), and was first discovered in the UK in Farningham , Kent in 2015 (Everatt, 2015; Malumphy, 2015). Since 2015 it has spread and is now found at multiple locations in London and the south east of England (Forestry Commission, 2018).

Control and management options for Oriental chestnut gall wasp have previously been reviewed (Everatt, 2015; Down and Audsley, 2016), the authors concluding that the only feasible control option for managing D. kuriphilus is a classical biological control programme involving the release of a non- native . There are 30 species of chalcid parasitoid wasps known to attack D. kuriphilus in China, but one in particular, Torymus sinensis Kamijo (Hymenoptera: Torymidae), was found to be a very common parasitoid of D. kuriphilus, and the strain native to China is phenologically synchronised with the life cycle of D. kuriphilus thus providing good control of the gall wasp populations (Moriya et al., 2003).

Torymus sinensis is univoltine. Adults emerge from D. kuriphilus galls in the early spring and oviposit inside fresh developing galls, on the surface of the gall wasp larvae. The T. sinensis larvae feed on the gall former and remain in the galls until the following spring.

Torymus sinensis has been released in Japan, North America and Italy to control Oriental chestnut gall wasp and has been very successful (detailed in Down and Audsley, 2016); up to 95% parasitisation rates have been reported in parts of Italy (Ferracini and Alma, 2015). More recently other European countries such as France (2011; Borowiec et al., 2014), Croatia (2014; Matošević et al., 2014) and Hungary (2014; Matošević et al., 2014), have followed suit. Torymus sinensis has also been introduced into areas of Slovenia although surveys have since indicated that the parasitoid may have arrived from other areas of Europe by natural spread prior to the first deliberate introduction in 2015 (Jurc et al., 2017). Test releases have been reported in Spain and Portugal (Paparella et al., 2016), and preparations are currently underway in the UK to gain approval for the use of T. sinensis to control Oriental chestnut gall wasp.

Prior to release of the exotic parasitoid wasp it is important to understand the native gall wasp communities and their intricately associated parasitoids and inquilines. An understanding of these communities may provide evidence of native parasitoid species with the potential to attack the invading gall wasp. Importantly, an understanding of these associations will also allow for effective monitoring of potential competition between the introduced parasitoid and native gall wasp parasitoids, which could occur if the host range of the introduced parasitoid is not limited to the invasive gall wasp species. Any such competition could be detrimental to native gall wasp communities. In Italy, damage to sweet resulting from gall wasp attack was severe so a quick decision was made to release T. sinensis in an effort to reduce the economic and environmental losses associated with the pest, with the first successful release conducted in 2005 (Quacchia et al., 2008). At that point in time, although T. sinensis was thought to be host specific, its host range had not been thoroughly investigated (Quacchia et al., 2008); monitoring for host range has instead been mainly post-release.

Parasitism levels in oak galls 4

Concerns have been previously raised over the continued use of T. sinensis as a biological control agent of Oriental chestnut gall wasp in Europe due to potential adverse effects, including the lack of information on its host range, potential hybridisation with native Torymus species, and the lack of evaluations on the direct and indirect non-target effects on the ecosytem (EFSA, 2010; Aebi et al., 2011; Gibbs et al., 2011). The European Food Safety Authority (EFSA, 2010) identified an undetermined risk that T. sinensis could parasitise native oak gall wasps and concluded that information on this risk was crucial before release occurred. Oak gall wasps have a very rich parasitoid community associated with them. This review identifies the oak gall wasp species present in the UK, provides detailed information on the life histories of these gall wasps, and details of their parasitoid wasp and inquiline associates. This review therefore aims to provide baseline information for these communites, which in conjunction with sampling in areas where D. kuriphilus is present (C. Malumphy, pers. comm.), will help to achieve effective monitoring for non-target effects and potential competition between T. sinensis and the native parasitoids of oak gall wasps, should the exotic parasitoid be released (or indeed, arrive naturally).

Parasitism levels in oak galls 5

Chapter 2. Cynipid oak galls of Great Britain

In 2010, EFSA concluded that there was undetermined risk (due to lack of investigation and evaluation) in relation to the potential ability of T. sinensis to parasitise native oak gall wasps (non-target effects); the EFSA panel also stated that gathering this information was crucial prior to release. This chapter therefore focuses on providing information about oak gall wasp species and their associated communities.

Oak gall wasps (Hymenoptera: Cynipidae) are typically characterised by their complex cyclically parthenogenetic life cycles (heterogony), alternating between sexual and asexual generations (Stone et al., 2002). There is a single sexual and asexual generation each year, usually with the whole sexual- asexual cycle completed in one year; typically (although there are many examples otherwise), the sexual generation develops in the spring or early summer while the asexual generation follows, developing during the summer and autumn (Stone et al., 2002). They are also characterised by their ability to induce a wide range of complex galls on (Quercus spp.) and other that are both species- and generation-specific (Stone et al., 2002). The majority of oak gall wasps form galls on the Quercus, but a few form galls on other hosts in the sub-family Castanoidea such as Castanaea spp. (Stone et al., 2002). Some species of and Callirhytis exhibit a phenomenon known as heteroecy whereby the sexual and asexual generations have different hosts (host alternation) (Stone et al., 2002); for example, some Andricus species (e.g. A. corruptrix, A. lignicola, A. kollari and A. quercuscalicis have a sexual generation that develops on hosts in the Cerris section (e.g. Q. cerris) whereas the asexual generation develops on hosts in the Quercus section (e.g. Q. robur and Q. petraea) (Schönrogge et al., 2000; Stone et al., 2002). In host alternating Callirhytis species it is the asexual generation that develops on Cerris section hosts whilst the sexual generation develops on Quercus section hosts (Stone et al., 2002).

Oak galls support a very rich and diverse, well-structured, community of parasitoids (super-family Chalcidoidea) and cynipid inquilines (tribe Synergini), most of which are obligately associated with the cynipid gall (Stone et al., 2002). Across Europe there are approximately 200 species of oak cynipids, approximately 100 species of chalcids (belonging to the Pteromalidae, Eulophidae, Torymidae, Eurytomidae, Eupelmidae and Ormyridae families) and 38 species of inquilines recorded as associated with cynipid galls (Hayward and Stone, 2005; Askew et al., 2013). Species of ichneumonid and braconid wasps are also known to attack oak cynipids however, the chalcid wasps are by far the most important both in terms of number of species and the level of mortality that they can inflict on the gall wasp (Weibes-Rijks and Shorthouse, 1992; Hayward and Stone, 2005). Williams (2010) report 41 hymenopteran species that cause galls on oaks in Great Britain. Table 1 (found at the end of this chapter) details the life-cycles, and associated parasitoids and inquilines, of 50 species of oak cynipids documented by Williams (2010) and others as present in Great Britain.

Cynipid oak galls and their communities have been the subject of much interest and observation in Britain (Niblett, 1944; Askew, 1961; 1965; 1966; Hails et al., 1990; Hails and Crawley, 1991; Schönrogge et al., 1995; 1996; 1998; 2000; 2002; Schönrogge and Crawley, 2000; Wurzell, 2000; Ellis 2002; 2004; 2005; 2006; Randolph, 2003). These publications provide a wealth of information on the gall formers, and the species of parasitoids and inquilines identified as being associated with the two generations of the gall wasp. Askew et al. (2013) collate these associations in one publication providing a very useful catalogue of the parasitoid and inquiline species associated with cynipid oak galls in the West Palaearctic; most of the associations detailed in Table 1 have come from this publication and have been supplemented with further information found elsewhere in the literature. However, despite all these publications, surprisingly few quantitative analyses of parasitoid and inquiline attack rates are

Parasitism levels in oak galls 6 reported. Most of the quantitative information on levels of attack provided in Table 1 has come from just two papers: Askew (1961) and Schönrogge and Crawley (2000). Some of this information is therefore dated and may not necessarily reflect the current situation. Data has also come from a limited number of sites across Great Britain. Nevertheless, it should still provide useful baseline information on levels of parasitism and inquiline infestation rates.

Data from Askew (1961) were primarily collected during a three-year study (1957-1960) when galls growing on Q. robur were collected in Wytham Wood, Berkshire, England, although a small portion of the data reflects associations that were not found in this location but instead are derived from other locations; hence this data is biased towards one site in the south-east of England, and one host species (Q. robur). Information is provided on the number of galls examined, and associations are quantitative in as far as the different thicknesses of arrows used by the author to denote the associations in the food webs represent ranges in the number of times an association was observed. This information has been used by ourselves to estimate percentage emergence rates, calculated as the number of individuals observed for each associated species as a proportion of the number of galls examined for each cynipid wasp species studied (Table 1). The linkage webs provided by Askew (1961) give further detail in that they identify specific associations within each gall type so for example, parasitoid attack has been separated out into attack on the gall maker itself and attack on any inquiline species present in the gall. The emergence rates provided in Table 1 do not make these distinctions, instead they provide an overall level of attack for each species; levels of attack were deliberately calculated in this way so that they could be compared with data obtained from a later quantitative study by Schönrogge and Crawley (2000) and data from Ferracini et al. (2017) both of which provide emergence rates and neither distinguish between the different associations.

Data from Schönrogge and Crawley (2000) comes from a two-year study (1994-1995) across eight sites in England and Scotland: two in south-east England, two in central England (one to the east, one to the west) and four ranging across Scotland. Their linkage webs present the data as absolute densities per area. i.e. number of host galls per 100m2 and number of individuals of any given species emerging per 100m2. The webs do not make any differentiations in the types of associations within the galls as the authors simply recorded the numbers of individuals that emerged from the galls rather than dissecting the galls to examine the intricacies of the associations. Another important point to make is that approximately only one third of the cynipid species found at the sites during a separate search were included in the webs because the remainder of the species were of very low density and effectively not detectable during the actual sampling of galls for their study. Therefore, Schönrogge and Crawley (2000) do not present any information in relation to the parasitoid and inquiline communities for the cynipid species that were less abundant at their sampling sites. The information within the Schönrogge and Crawley (2000) linkage webs has been used by ourselves to estimate approximate percentage emergence rates, calculated as the number of individuals observed for each associated species per 100m2 as a proportion of the number of galls per 100m2 for each cynipid species studied (Table 1).

Four invasive gall species, Andricus corruptrix, A. quercuscalicis, A. lignicola and A. kollari have been more extensively studied with investigations focussing on the colonisation, dispersal and subsequent recruitment of native parasitoids and inquilines. These species have invaded Great Britain over the last 150 years or so (either naturally or human-assisted): (first imported into Britain in the mid-1800s); A. quercuscalicis arrived in the British Isles during the late 1950s; A. lignicola in the mid-1960s and A. corruptrix was first reported in the early 1970s (Schönrogge et al., 2000). All four of these species have a spring sexual generation that is restricted to Q. cerris (itself non-native to Britain) and an asexual generation that develops on Q. robur and Q. petraea, and therefore their dispersal and

Parasitism levels in oak galls 7 distribution are defined by areas where Q. cerris is present. All four species have spread westwards and northwards since their arrival; A. quercuscalicis, A. kollari and A. lignicola are now common and widespread through England and Wales (Schönrogge et al., 2000; Redfern et al., 2002) whereas populations of A. corruptrix are locally common, although scattered, but spreading rapidly (Redfern et al., 2002).

Hails and Crawley (1991) report a fairly constant rate of parasitism (20-30%) of the sexual generation of A. quercuscalicis by four species of Mesopolobus (M. dubious, M. fuscipes, M. tibialis and M. xanthocerus) during a study that ran over eight years (1981-1989) at a single location in England (Silwood Park, Berkshire). These authors found no parasitism of the asexual generation during their study (1000 galls sampled per year) but state that very low levels of parasitism from nearby locations had been recorded. Hails et al. (1990) compiled all records of parasitism pertaining to the asexual generation of A. quercuscalicis from Britain, and the reader is directed to this publication for detail; they concluded that rates of parasitism of the asexual gall were still very low in Britain at that point in time (in most cases < 5%, with even lower frequencies of inquilines) but that there was an indication that they could be slightly increasing (a figure of 5.1% parasitism is reported for a 1994 publication cited within Randolph (2003). As part of their review, these authors compared parasitism of this gall in Britain with information from France where the gall wasp is a native. In France, the knopper gall supports a diverse range of parasitoids, many of which are also native to the UK (Hails et al., 1990), and a parasitism rate of 13.6% on the continent has been quoted (within Randolph 2003). In contrast, Schönrogge et al. (2000) report a 773% total attack rate (adults emerged per gall), made up of a composition of seven parasitoid species and three inquiline species, of the asexual generation of A. quercuscalicis in a survey conducted in 1994, also in Silwood Park1.

Randolph (2003) published results of a study based in the west of England (Bristol) during 2000-2002 investigating parasitism of knopper galls. Overall, 68.5% of the total number of galls collected were not parasitized. Randolph (2003) report Cecidostiba fungosa as being the most commonly found parasitoid emerging from knopper galls with a parasitism rate of 48.1-258% per gall, followed by M. sericeus (6.0-27.3%), Eurytoma brunniventris (1.3-4.0%), Eupelmus urozonus (1.3–2.0%) and Torymus auratus (1.3%); C. fungosa made up 60.6-94.9 % of all the emerged parasitoids with M. sericeus making up 2.2-34.4% over the two years. Only two species of inquilines emerged from the galls, the predominant one being Synergus facialis (infestation rates of 1.08-11.0%) with just one specimen of S. pallipes observed. All the parasitism observed was on S. facialis rather than the gall inducer, and when taking into account the total number of inquiline eggs laid (inquiline attack rate), parasitism of the inquiline larvae across all sites and years averaged out to 29.4% and is comparable to a figure previously calculated for these galls on the continent where C. fungosa is also the dominant parasitoid (Randolph 2003). This contrasts with another (much larger) study (across 20 sites in Great Britain and seven sites in Ireland he UK) where M. sericeus was found to be the dominant parasitoid; M. sericeus parasitism on the inquilines was in the region of 65-90%, other parasitoid species (E. brunniventris and E. urozonus) were observed but no C. fungosa emerged (cited within Randolph, 2003).

1 Although the asexual generation galls of A. quercuscalicis are unilocular, and the recorded parasitoid species are solitary ecto/endoparastioids, most of the parasitoid species can attack the gall inducer, inquilines or other parasitoid species already present within the gall. The inquiline species recorded from these galls are potentially gregarious within the host gall. Therefore, the number of parasitoids (attacking inquilines) or inquilines emerging per gall can be > 1 resulting in percentage attack rates (= (number of parasitoids and inquilines/number of galls)*100) exceeding 100%.

Parasitism levels in oak galls 8

The number of parasitoid species associated with the knopper gall has increased since 1990 (Table 2; Schönrogge et al., 2000; Schönrogge and Crawley, 2000; Randolph, 2003) and this has been explained as corresponding with the colonisation of these galls by Synergus spp. (inquilines), providing additional resources within the galls for exploitation by chalcid parasitoids (Hails et al., 1990; Schönrogge et al., 1996). Hails et al. (1990) report that to a large extent, many of the parasitoid species found in French knopper galls were attacking the inquiline species rather than the gall inducer. In addition, larvae of the gall inducer are found in an inner cavity consisting of a thin-walled oval chamber protected by the outer wall of the gall which is thick, convulated and corky (Hails et al., 1990; Randolph, 2003). This provides the gall maker with a degree of protection from parasitoid attack. Randolph (2003) suggests that the community within these galls is converging towards the community structure known to occur in continental Europe.

Schönrogge et al. (2000) published parasitoid attack rates for A. corruptrix, A. quercuscalicis, A. lignicola and A. kollari from data obtained from the same sites described in Schönrogge and Crawley (2000). Only Mesopolobus species of parasitoids (M. dubius, M. fuscipes, M. tibialis and M. xanthocerus) were observed attacking the sexual generations. In contrast, with the exception of A. lignicola (which was only attacked by S. facialis and S. reinhardii), a greater number of parasitoids and inquilines attacked the asexual generations of these invading cynipids; parasitoid attack rates (percentage of galls attacked by parasitoid species) for the sexual generation and the percentage of parasitoids and inquilines that emerged per gall for the asexual generations across all sites where the galls were found are provided in Table 2.

Table 2. Parasitoid attack rates (percentage of galls attacked by parasitoid species) for the sexual generation and the percentage of parasitoids and inquilines that emerged per gall for the asexual generations of four invasive species of Andricus as reported by Schönrogge et al. (2000) across all sites where these galls were found in their study.

Andricus Andricus Andricus kollari corruptrix quercuscalicis Sexual 0 – 75 % 11 – 45 % 12 – 46 % 5 – 77 % generation Agamic 41.4 – 51 % 3.4 – 932 % 1 – 2.9 % 14.7 – 395 % generation

The surveys reported by Schönrogge et al. (2012) suggest that the parasitoid and inquiline species associated with the four early invaders have remained largely unchanged since a previous survey in 1994/1995 (Schönrogge et al., 2000) whereas the parasitoid assemblages associated with the more recent invasive species of Andricus (A. lucidus, A. aries, A. grossulariae) and the invasive cerricola are developing rapidly.

It is widely reported that attack by parasitoids and inquilines (and other predators) can result in high levels of mortality in gall wasps (Stille, 1984; Wiebes-Rijks and Shorthouse, 1992; Stone et al., 1995; 2002; Schönrogge et al., 1999) however, Stone et al. (2002) point out that few studies have actually demonstrated significant top-down effects (i.e. an effect imposed from a higher trophic level downwards), and most have been inconclusive. Wiebes-Rijks and Shorthouse (1992) suggest that rates of parasitism in galls often exceed 80%. The majority of parasitoid species associated with cynipid gall wasps will only attack gall wasps on oak although there are exceptions: Eupelmus urozonus (and E. vesicularis) are highly polyphagous, attacking a range of hosts across different plant Orders, and biguttata, S. flavicollis, Torymus auratus, Mesopolobus sericeus and Aulogymnus skianeuros

Parasitism levels in oak galls 9 have been reported to attack galls on other (usually Rosa spp.) (Stone et al., 2002). Those restricted to oak are often polyphagous with a broad host range, often attacking several different cynipid gall wasp species along with other chalcid species of parasitoid (Askew et al., 2013); very few parasitoids are restricted to just one species of oak gall wasp (Wiebes-Rijks and Shorthouse, 1992; Stone et al., 2002). Eurytoma brunniventris (100 host species), pomaceus (96 host species), Eupelmus urozonus (87 host species), and S. biguttata (80 host species) have the highest number of hosts across the west Palaearctic (Askew et al., 2013) whilst Torymus flavipes (with 38 host gall species across the west Palaearctic region) was found to be the most commonly reared parasitoid in the Askew et al. (2013) compellation, followed by S. biguttata, A. skianeuros (19 host species), Cecidostiba fungosa (64 host species), E. brunniventris, Torymus affinis (7 host species), Megastigmus dorsalis (65 host species), T. auratus (41 host species), Aulogymnus gallarum (42 host species), Mesopolobus xanthocerus (40 host species), O. pomaceus and Aulogymnus obsuripes (9 host species).

The asexual and sexual generations of cynipid galls usually have different species of parasitoids associated with them (Askew, 1961; Schönrogge and Crawley, 2000; Table 1) but galls of the same generation of closely related oak cynipids often have similar associated species (Askew, 1961; Table 1) for example, asexual galls of divisa and C. longiventris share similar communities as do both sexual and asexual generation galls of quercusbaccarum, N. numismalis and N. albipes.

Cynipid inquilines inhabitat the galls, living commensally within them, but do not themselves induce primary gall formation (Askew, 1961) although they are still able to induce the development of larval chambers (Hayward and Stone, 2005). Inquiline species can be classified as nonlethal or lethal. Non- lethal inquilines induce their larval chambers in peripheral gall tissue and do not interfere with the development of the gall wasp larva whereas the lethal inquilines develop within the chambers of the gall inducer, killing the gall wasp in the process (hence are not commensal in the true sense of the word); the latter can cause local extinctions of gall inducers (Stone et al., 2002; Hayward and Stone, 2005). Askew (1961) and Wiebes-Rijks and Shorthouse (1992) both describe Synergus pallicornis as a non-lethal inquiline and Askew (1961) also reports S. umbraculus as a non-lethal inquiline whereas other species of Synergus construct subsidiary cells within the galls that encroach upon the chamber of the gall maker, destroying its contents.

Parasitism levels in oak galls 10

Table 1. Species of oak gall wasps present in Great Britain, detailing host plants, life-cycle parameters, distribution within the British Isles, and hymenopteran associates.

British host plants are listed first in the ‘Host plant’ column, with other species of oak known to be hosts included in the second list within this column.

Known parasitoid and inquiline associations in the western Palaearctic region are provided in column six. Associations that have been confirmed in Great Britain and/or Italy are indicated in column seven along with the host plant that these associations have been found on (if known). Associate species given in parantheses are likely to be only incidentally associated and those whose identity are uncertain are indicated with a question mark (Askew et al., 2013).

Percent level of parasitism refers to the percent emergence rate (ER) of parasitoids and is calculated (as number of parasitoids/total number of galls)*100. It is a measure of the relative parasitoid abundance per gall and therefore is not a measure of exact percentage parasitism (Kos et al., 2015) but it does allow determination of relative parasitoid abundance. Emergence rates are more reliable if the sample number of galls is large; when sample numbers are low the rate is easily skewed. Percent inquiline infestation rate (IR) is calculated as (number of inquilines that emerged from the galls/total number of galls)*100 and therefore gives a measure of emergence rates rather than inquiline attack rates (which would indicate the number of eggs laid by the attacking inquiline). Ranges of ER and IR given for the Schönrogge and Crawley (2000) data represent spatial range i.e. the range in rates across all the sample sites where the gall species was found and studied. A superscript ‘a’ indicates that the figure could be an overestimate; the linkage webs in the original paper did not provide exact proportions when the host gall contributed less than 5% of a parasitoid/inquiline population therefore a proportion of 5% has been assumed in these instances for our calculations. Mean ER and IR for each associated parasitoid/inquiline across the sampled sites are provided in parantheses after the range. Schönrogge and Crawley (2000) and Ferracini et al. (2017) data for parasitoid emergence rates and inquiline infestation rates are totalled for each gall wasp species, with the mean total rates (across all sampling sites where the gall wasp was found) provided for the Schönrogge and Crawley (2000) data. Ranges of parasitoid emergence rates and inquiline infestation rates for the Askew (1961) data are not a spatial range but reflect the way that the original data was represented in the schematic food webs drawn up by the author and represents a minimum to maximum rate (see earlier text for full explanation); total ER and IR are therefore not provided for this data as they could not be calculated from the original paper. N/A in the Askew (1961) and Schönrogge and Crawley (2000) data columns indicates that there is no evidence for that particular parasitoid/inquiline association with the gall wasp species in question. It should be noted that levels of parasitism from Ferracini et al. (2017) refer to data collected after the release of T. sinensis.

Further useful information (when available) pertaining to each gall wasp species are provided as footnotes. On occasions, these include the percentage representations of inquilines given by Askew et al. (2013) from galls where an excess of 700 inquilines and chalcids have been recorded. However, it is unclear how wide a sample area this data is from; it is likely that it is collated from data across the whole of the west Palaearctic as this is the area covered by the publication. These footnotes also include information from Ferracini et al. (2017) pertaining to parasitism by T. sinensis (if observed).

Parasitism levels in oak galls 11

Oak Gall Wasp Common Host plant Life history (in Status in Great Associated Present in Level of parasitism (%) / Inquiline References species name of Great Britain) Britain parasitoids and Great infestation rate (%) gall inquilines Britain or Italy? Askew Schönrogge Ferracini (1961) and et al. Crawley (2017) (2000) Andricus Q. petraea Galls on catkins Ellis (2018) albopunctatus Q. robur (Schlechtendal)2 Q pubescens (= Andricus paradoxus (Radoszkowski))

Sexual generation Andricus Spotted- Q. petraea Galls found May Quite common Eurytoma GB (Q. 13.9 - No data No data Redfern et al. albopunctatus Gall Q. robur to June on brunniventris robur) 30.6 available available (2002); BRC- (Schlechtendal) vegetative ; Caenacis lauta GB (Q. 5.5 - 13.9 for this for this DBIF (2008); Q pubescens mature end of robur) species species Williams (= Andricus June Mesopolobus GB None (2010); Askew paradoxus amaenus observed et al. (2013); (Radoszkowski)) Adults emerge Mesopolobus N/A Ellis (2018); March to April of fasciiventris Nature Spot Asexual generation 2nd year Mesopolobus GB None (2019) sericeus observed Mesopolobus tibialis GB (Q. 22.2 - robur) 69.4

Eupelmus urozonus GB (Q. 5.6 - 13.9 robur) sp. N/A

Inquilines:

2 Only the asexual generation of A. albopunctatus is listed in Williams (2010) and Askew et al. (2013) implying that the sexual generation is not known in Great Britain/West Palaearctic region.

Parasitism levels in oak galls 12

Ceroptres clavicornis N/A Synergus facialis GB > 55.5 Synergus pallicornis N/A Synergus pallipes GB None observed Synergus radiatus GB None observed Andricus amenti Q. petraea Galls found May Rare Mesopolobus No No data No data No data Redfern et al. Giraud Q. robur to June amaenus parasitoids available available available (2002); BRC- on ; Mesopolobus tibialis or for this for this for this DBIF (2008); Sexual generation Q. pubescens mature end of Mesopolobus inquilines species species species Williams June xanthocerus known to (2010); Askew Eupelmus urozonus be et al. (2013); Adults emerge Aulogymnus associated Ellis (2018) May to July gallarum in the UK Aprostocetus aethiops Aprostocetus sp.

No known inquilines Andricus amenti Hairy- Q. petraea Not recorded in Eurytoma No No data No data No data Redfern et al. Giraud Catkin Q. robur Great Britain brunniventris parasitoids available available available (2002); BRC- Gall or for this for this for this DBIF (2008); Asexual generation Q. pubescens Mesopolobus inquilines species species species Askew et al. (= giraudianus) fasciiventris known to (2013); Ellis Eupelmus urozonus be (2018) associated Inquilines: in the UK Synergus pallipes Andricus aries Rams- Q. petraea Galls found July Common around Eurytoma adleriae No data No data Redfern et al. (Giraud)3 Horn Gall Q. robur to December on London and Eurytoma GB/IT available available 9.7 (2002); Stone buds; mature in other parts of brunniventris for this for this et al., (2002); Asexual generation Q. pubescens August the south east of Sycophila biguttata GB/IT species species 7.2 Williams England; rapidly Sycophila flavicollis GB (2010); expanding range Sycophila variegata GB/IT 3.2 Schönrogge et

3 Andricus aries is an invasive species, introduced into Great Britain in 1997. No sexual generation is known. Wurzell (2000) reports one specimen of M. dorsalis (ER = 2.0%) and an unknown number of S. facialis (up to 20 specimens, infestation rate < 38%) emerging from a total of 50 galls taken from one location.

Parasitism levels in oak galls 13

Adults emerge and now found Megastigmus GB/IT 9.7 al. (2012); August to in north west dorsalis Askew et al. October and April England Megastigmus GB (2013) to May (Cheshire) ?stigmatizans Torymus flavipes GB GB Ormyrus pomaceus IT 2.4 Ormyrus spp. 8.9 Caenacis lauta Cecidostiba fungosa GB Eupelmus azureus IT 4.0 Eupelmus spongipartus Eupelmus urozonus IT 0.8 Total ER = 47.3 Inquilines: Ceroptres clavicornis GB (Q. robur) Synergus facialis GB Synergus hayneanus Synergus pallicornis GB Synergus pallipes GB Synergus GB pallidipennis Synergus reinhardi GB Synergus tibialis GB Synergus GB rotundiventris Synergus umbraculus Andricus callidoma Tufted Q. petraea Galls found end Rare Torymus flavipes N/A No data No data Redfern et al. (Hartig) Gall Q. robur of April to May Mesopolobus N/A available available (2002); on flowers; fasciiventris for this for this Williams Sexual generation Q. pubescens mature in May Mesopolobus GB (Q. None species species (2010); Askew (= cirratus) fuscipes robur) observed et al. (2013); Mesopolobus tibialis N/A Ellis (2018)

Parasitism levels in oak galls 14

Adults emerge Mesopolobus GB (Q. None May to June xanthocerus petraea) observed Mesopolobus sp. GB 4.5 (Pteromalus chrysos N/A & P. spp.) Eupelmus urozonus N/A Aulogymnus GB (Q. None gallarum petraea) observed Aprostocetus N/A aethiops

No known inquilines Andricus callidoma Stalked- Q. petraea Galls found May Uncommon Eurytoma GB (Q. 30.8 - No data No data Redfern et al. (Hartig) Spindle Q. robur to October on (local) brunniventris robur) 76.9 available available (2002); Gall vegetative buds; Ormyrus pomaceus N/A for this for this Williams Asexual generation Q. pubescens mature end of Caenacis lauta N/A species species (2010); Askew August Mesopolobus GB (Q. None et al. (2013); fasciiventris petraea) observed Ellis (2018) Adults emerge Mesopolobus GB (Q. 15.4 - March to April of sericeus robur) 38.5 2nd year (Pteromalus N/A chrysos) Eupelmus N/A spongipartus Eupelmus urozonus N/A

Inquilines: Ceroptres clavicornis N/A Synergus facialis GB (Q. 30.8 - robur) 76.9 Synergus pallipes GB (Q. None robur) observed Synergus radiatus N/A Synergus N/A thaumacerus

Parasitism levels in oak galls 15

Andricus corruptrix Q. cerris Galls found Rare and Mesopolobus dubius GB (Q. No data 0 – 18 (8.5) No data Redfern et al. (Schlechtendal)4 February to June scattered cerris) available available (2002); BRC- on vegetative (increasing Mesopolobus GB (Q. for this 37.5 – 714a for this DBIF (2008); Sexual generation buds; mature in rapidly) fuscipes cerris) species (265.5) species Williams (= larshemi) late March Mesopolobus tibialis GB 0 – 36a (12) (2010); Askew Mesopolobus GB (Q. 0 - 3.3 (1.1) et al. (2013); Adults emerge xanthocerus cerris) Ellis (2018) mid-April to May Eupelmus urozonus GB 0 – 1 (0.33) Mean total ER = 287.4 No known inquilines Andricus corruptrix Q. petraea Galls found May Locally common, Eurytoma GB (Q. No data 25a – 50a No data Redfern et al. (Schlechtendal) Q. robur to July and spreading brunniventris robur) available (37.5) available (2002); BRC- onwards on rapidly for this for this DBIF (2008); Asexual generation Q. canariensis vegetative buds; species species Williams Q. montana mature in July Eurytoma setigera N/A (2010); Askew Q. pubescens Sycophila biguttata GB 0 – 5a (2.5) et al. (2013); Adults emerge in Sycophila variegata GB None Ellis (2018); October of 1st observed Nature Spot year and July to Megastigmus GB (Q. None (2019) August of 2nd dorsalis robur) observed year Torymus auratus GB 0 -25a (12.5) Torymus flavipes GB (Q. None robur) observed Ormyrus nitidulus N/A Ormyrus pomaceus GB (Q. 1 -70 (35.5) robur) Ormocerus latus N/A Caenacis lauta N/A Cecidostiba fungosa GB (Q. 0 – 70 robur) (35.5) Mesopolobus GB (Q. 0 – 285 amaenus robur) (142.5)

4 Andricus corruptrix is an invasive species, first recorded in 1976. Schönrogge et al. (1998) report that 0 - 66% of A. corruptrix sexual generation galls were parasitized in their 1994/1995 study.

Parasitism levels in oak galls 16

Mesopolobus dubius GB None observed Mesopolobus GB (Q. 0 – 10 (5) fasciiventris robur) Mesopolobus GB None fuscipes observed Mesopolobus GB (Q. 0 – 50a (25) sericeus robur) Mesopolobus tibialis GB None observed Eupelmus N/A spongipartus Eupelmus urozonus GB (Q. None robur) observed Mean total ER = 295.5 Inquilines: Ceroptres clavicornis GB None observed Synergus apicalis GB None observed Synergus facialis GB (Q. 0 – 150 (75) robur) Synergus pallicornis N/A Synergus pallipes N/A Synergus radiatus N/A Synergus reinhardi GB (Q. 0 – 50 (25) robur) Synergus tibialis N/A Synergus GB None umbraculus observed Mean total IR = 100.0 Curved- Q. petraea Galls found May Common and Eurytoma GB (Q. 2.2 - 5.5 0 - 3.3 2.2 Redfern et al. Hartig5 Leaf Gall Q. robur to July and widespread brunniventris robur); IT (0.76) (2002); BRC-

5 Askew et al. (2013) report a percentage representation of inquilines of 12% in the sexual generation galls of A. curvator. Ferracini et al. (2017) report that galls of the sexual generation of A. curvator are attacked by T. sinensis in the field (see Table 3 for further details).

Parasitism levels in oak galls 17

onwards on Eurytoma pistaciae IT N/A N/A 0.2 DBIF (2008); Sexual generation Q. canariensis vegetative buds, Eurytoma setigera N/A N/A Williams Q. cerris leaves and stems; Sycophila biguttata IT N/A N/A 0.2 (2010); Askew Q. faginea mature in July Sycophila variegata N/A N/A et al. (2013); Q. frainetto Megastigmus GB None None Ellis (2018); Q. x Adults emerge dorsalis observed observed NatureSpot haynaldiana May to August Torymus ?affinis N/A N/A (2019) Q. x hispanica Torymus auratus GB 3.7 - 6.3 None Q. infectoria observed Q. ithburensis Torymus cingulatus GB 0.4 None Q. lusitanica observed Q. pubescens Torymus flavipes GB (Q. None 0 - 14.3a 2.6 Q. pyrenaica robur); IT observed (3.67) (Q. robur) Torymus geranii GB (Q. None 0 - 3.8 robur) observed (0.53) Torymus notatus GB (Q. > 7.3 None robur) observed Torymus spp. 0.2 Torymus spp. 0 - 14.3a (males) (3.74) Ormyrus nitidulus N/A N/A Ormyrus pomaceus IT N/A N/A 0.2 Ormyrus spp. IT N/A N/A 0.4 Pteromalus IT N/A N/A 0.1 bedeguaris Pteromalus sp. N/A N/A Cecidostiba fungosa N/A N/A Cecidostiba IT N/A N/A 0.2 semifascia Hobbya stenonota N/A N/A Mesopolobus GB (Q. None None albitarsus robur) observed observed Mesopolobus GB (Q. None None amaenus robur) observed observed Mesopolobus dubius N/A N/A Mesopolobus GB (Q. None 0 – 1 (0.31) fasciiventris robur); IT observed (Q. robur)

Parasitism levels in oak galls 18

Mesopolobus GB (Q. None None fuscipes robur) observed observed Mesopolobus GB (Q. None 0 - 1.3 (0.2) 0.1 sericeus robur); IT observed Mesopolobus N/A N/A tarsatus Mesopolobus tibialis GB (Q. None 0 - 2.9a 0.3 robur); IT observed (0.70) Mesopolobus N/A N/A xanthocerus Mesopolobus sp. GB 1.1 Eupelmus kiefferi IT N/A N/A 0.3 Eupelmus N/A N/A spongipartus Eupelmus urozonus GB (Q. 0.4 None 1.9 robur); IT observed Eupelmus vesicularis N/A N/A Eupelmus spp. 0.2 Aulogymnus GB (Q. > 7.3 None 3.1 arsames robur); IT observed Aulogymnus GB (Q. 0.4 None 0.2 gallarum robur); IT observed Aulogymnus N/A N/A gallarum f. pulchra Aulogymnus N/A N/A skianeuros Aprostocetus N/A N/A aethiops Baryscapus spp. IT N/A N/A 0.1 Mean total Total ER ER = 9.9 = 12.5 Inquilines: Ceroptres clavicornis N/A N/A Saphonecrus N/A N/A connatus Synergus apicalis N/A N/A Synergus GB (Q. 0.7 - 1.8 None crassicornis robur) observed

Parasitism levels in oak galls 19

Synergus facialis GB None 0 – 2 (0.51) observed Synergus incrasatus N/A N/A Synergus pallicornis GB None 0 – 1 (0.13) observed Synergus pallipes GB None 0 - 43.7 observed (0.951) Synergus radiatus GB/IT None None observed observed Synergus ruficornis N/A N/A Synergus N/A N/A thaumacerus Synergus tibialis GB (Q. None None robur) observed observed Synergus GB 2.9 - 9.2 None facialis/pallipes observed Mean total IR = 10.1 Andricus curvator Collared- Q. petraea Galls found Common Ormyrus pomaceus N/A No data No data Redfern et al. Hartig Bud Gall Q. robur August to Mesopolobus GB (Q. 10 available available (2002); BRC- September on amaenus robur) for this for this DBIF (2008); Asexual generation Q. canariensis vegetative buds; Mesopolobus GB (Q. None species species Williams (= collaris) Q. faginea mature end of fasciiventris petraea) observed (2010); Askew Q. x hispanica September Mesopolobus N/A et al. (2013); Q. pubescens sericeus Ellis (2018) Q. pyrenaica Adults emerge March to April Inquilines: the following Synergus facialis GB spring Synergus incrasatus N/A Synergus pallicornis N/A

Synergus radiatus GB Synergus ruficornis N/A Synergus tibialis N/A Synergus sp. 20 Andricus fecundator Hairy- Q. petraea Galls found May Common Mesopolobus GB > 20 No data No data Redfern et al. (Hartig) Catkin Q. robur to June on xanthocerus available available (2002); BRC- (= foecundatrix) Gall flowers; mature for this for this DBIF (2008); Q. faginea end of May species species Williams

Parasitism levels in oak galls 20

Sexual generation Q. frainetto No known inquilines (2010); Ellis (= pilosus) Q. infectoria Adults emerge (2018) and subsp. May to August veneris Q. lusitania Q. pubescens Q. pyrenaica Andricus fecundator Artichoke Q. petraea Galls found June Common and Eurytoma IT N/A No data 0.7 Redfern et al. (Hartig) or hop Q. robur to September on widespread brunniventris available (2002); BRC- (= foecundatrix) gall vegetative buds; Megastigmus GB/IT None for this 1.6 DBIF (2008); Q. faginea mature end of dorsalis observed species Williams Asexual generation Q. frainetto July Torymus auratus GB/IT None 1.0 (2010); Ellis Q. x hispanica observed (2018); Q. lusitanica Adults emerge Cecidostiba fungosa IT N/A 0.3 NatureSpot Q. pubescens March to April Ormyrus pomaceus IT N/A 0.3 (2019) Q. pyrenaica from 1-3 years Ormyrus spp. IT N/A 0.3 owards Eupelmus azureus IT N/A 1.6 Eupelmus urozonus GB 1.4 Aulogymnus GB 1.4 trilineatus Total ER = 5.9 Inquilines: Synergus GB None crassicornis observed Andricus Q. cerris Not present in Eurytoma No data No data Askew et al. gallaeurnaeformis Q. frainetto Great Britain? brunniventris available available (2013); Ellis (Boyer de Q. lusitanica Eurytoma setigera for this for this (2018) Fonscolombe)6 Q. petraea Sycophila biguttata species species Q. pubescens Torymus ?affinis Asexual generation Q. robur Torymus ?notatus Q. rubra Ormyrus pomaceus Caenacis lauta Cecidostiba fungosa Mesopolobus fasciiventris

6 No information is available for A. gallaeurnaeformis in Redfern et al. (2002), BRC-DBIF (2008) or Williams (2010) suggesting that it is absent in Great Britain.

Parasitism levels in oak galls 21

Eupelmus spongipartus Eupelmus urozonus IT 4.5 Aulogymnus gallarum Aprostocetus sp. Total ER = 4.5 Inquilines:

Ceroptres clavicornis Synergus facialis Synergus incrassatus Synergus pallipes Synergus tibialis Andricus gemmeus Q. cerris No information No data No data No data Schönrogge et (Giraud)7 available available available available al. (2012) for this for this for this Sexual generation species species species Andricus gemmeus Q. petraea Eurytoma No No data No data No data Schönrogge et (Giraud)8 Q. robur brunniventris parasitoids available available available al. (2012) Sycophila biguttata or for this for this for this Asexual generation Ormyrus nitidulus inquilines species species species Orymrus pomaceus known to Mesopolobus be fasciiventris associated Eupelmus urozonus in the UK

Inquilines: Ceroptres clavicornis Synergus fascialis

7-7 Andricus gemmeus is an invasive species, which was first observed in Essex in 2008 (Bowdrey, 2009).

Parasitism levels in oak galls 22

Andricus Q. petraea Galls found on BRC-DBIF gemmicola Kieffer9 Q. robur vegetative buds (2008); Ellis (2018) Sexual generation Q. pubescens

Andricus glandulae Q. petraea Galls found April Rare and Eurytoma No No data No data No data Redfern et al. (Hartig) Q. robur to May on scattered brunniventris parasitoids available available available (2002); BRC- flowers; matured Torymus flavipes or for this for this for this DBIF (2008); Sexual generation by June Mesopolobus tibialis inquilines species species species Williams (=xanthopus) Mesopolobus known to (2010); Askew Adults emerge xanthocerus be et al. (2013); May to June of Pteromalus sp. associated Ellis (2018) 2nd year Aprostocetus in the UK aethiops

No known inquilines Andricus glandulae Thatched Q. petraea Galls found July Rare and Eurytoma N/A No data No data Redfern et al. (Hartig) Gall Q. robur (only to September on scattered brunniventris available available (2002); BRC- rarely) shoots and Sycophila biguttata N/A for this for this DBIF (2008); Asexual generation vegetative buds; Ormyrus pomaceus N/A species species Williams Q. lusitanica mature in (2010); Askew Q. pubescens September Inquilines: et al. (2013); Q. pyrenaica Ceroptres clavicornis N/A Ellis (2018) Adults emerge Saphonecrus N/A st October of 1 connatus year and March Synergus facialis GB None nd to April of 2 observed year Synergus pallipes GB None observed Synergus radiatus GB None observed Q. robur Galls found in Rare (newly Eurytoma adleriae No data No data Redfern et al. Q. cerris May on flowers introduced) Eurytoma GB (Q. available available 3.9 (2002); Stone brunniventris cerris)/IT for this for this et al., (2002); Q. frainetto Adults emerge Southern and Eurytoma pistaciae IT species species 2.0 Williams Q. x hispanica June to July eastern England Eurytoma setigera (2010);

9 Ellis (2018) state that the species A. gemmicola is questionable. No information is available for this species in Williams (2010) or Askew et al. (2013).

Parasitism levels in oak galls 23

Andricus Q. infectoria Sycophila biguttata GB (Q. 5.9 Schönrogge et grossulariae and supsp. cerris)/IT al. (2012); Giraud10 veneris Sycophila flavicollis GB (Q. Askew et al. Q. ithaburensis cerris) (2013); Ellis Sexual generation Q. suber Sycophila variegata GB (Q. 1.0 (2018) Q. trojana cerris)/IT Megastigmus GB (Q. 5.9 dorsalis cerris)/IT Torymus auratus Torymus flavipes GB (Q. 3.9 cerris)/IT Torymus geranii Ormyrus nitidulus GB (Q. cerris) Ormyrus pomaceus GB (Q. cerris)/IT Ormocerus latus Cyrtoptyx robustus Cecidostiba fungosa GB (Q. 8.8 cerris)/IT Cecidostiba semifascia Hobbya stenonata Mesopolobus GB (Q. 1.0 amaenus cerris)/IT Mesopolobus dubius GB Mesopolobus fasciiventris Mesopolobus GB (Q. fuscipes cerris) Mesopolobus lichtensteini Mesopolobus GB (Q. sericeus cerris)

10 Andricus grossulariae is an invasive species and was at first only found on Q. cerris in Great Britain (Walker, 2001) but is now known not to be wholly dependent on Q. cerris (Schönrogge et al., 2012). Askew et al. (2013) report a percentage representation of inquilines of 47% for sexual generation galls.

Parasitism levels in oak galls 24

Mesopolobus tibialis GB (Q. cerris)/IT Mesopolobus GB (Q. xanthocerus cerris) Mesopolobus spp. IT 1.0 Eupelmus azureus IT 2.0 Eupelmus spongipartus Eupelmus urozonus GB (Q. cerris) Aulogymnus IT 2.0 gallarum Aulogymnus obscuripes Aulogymnus skianeuros Aulogymnus testaceoviridis Aulogymnus trilineatus Aprostocetus aethiops Aprostocetus cerricola Aprostocetus domenichinii Pediobius rotundatus ( planatus) GB Total ER = 39.2 Inquilines: Ceroptres cerri Saphonecrus haimi Saphonecrus undulatus Synergus IT consobrinus

Parasitism levels in oak galls 25

Synergus facialis GB (Q. cerris) Synergus thaumacerus Synergus variabilis Andricus Q. petraea Galls on acorn Newly Eurytoma adleriae IT No data No data Redfern et al. grossulariae Q. robur cups; mature in discovered Eurytoma GB/IT available available 25 (2002); Stone Giraud11 the autumn brunniventris for this for this et al., (2002); Q. faginea Eurytoma setigera species species Williams Asexual generation Q. frainetto Adults emerge Sycophila biguttata GB/IT 43.8 (2010); Askew (= mayri) Q. infectoria January to April Megastigmus GB/IT 193.8 et al. (2013); Q. lusitanica in 2nd year dorsalis Ellis (2018) Q. pubescens Megastigmus IT Q. pyrenaica stigmatizans Torymus auratus Ormyrus nitidulus GB/IT 6.25 Ormyrus pomaceus IT Caenacis lauta Cecidostiba fungosa GB/IT 18.8 Cecidostiba semifascia

Cyrtoptyx robustus Hobbya stenonota Mesopolobus amaenus Mesopolobus GB sericeus

Mesopolobus tibialis GB Mesopolobus GB xanthocerus

Eupelmus spongipartus

11 Andricus grossulariae is an invasive species and was at first only found on Q. cerris in Great Britain (Walker, 2001) but is now known not to be wholly dependent on Q. cerris (Schönrogge et al., 2012). Askew et al. (2013) report a percentage representation of inquilines of 10% for asexual generation galls.

Parasitism levels in oak galls 26

Eupelmus urozonus GB/IT Eupelmus vesicularis Aulogymnus gallarum Aulogymnus IT skianeuros Aulogymnus trilineatus Aprostocetus aethiops

Baryscapus anasillus Baryscapus berhidanus Baryscapus ?diaphantus Baryscapus ?pallidae (Scambus planatus) GB (Q. robur) (Bracon kopelkei) GB (Q. robur) Total ER = 287.5 Inquilines: Synergus IT crassicornis Synergus facialis GB Synergus hayneanus Synergus pallicornis Synergus pallidipennis Synergus pallipes GB Synergus GB/IT umbraculus Twig Gall Q. petraea Galls found all Moderately Sycophila biguttata IT N/A No data 0.2 Redfern et al. Q. robur year round on common Sycophila variegata IT N/A available 0.4 (2002); BRC-

Parasitism levels in oak galls 27

Andricus inflator vegetative buds Megastigmus GB (Q. 2.9 for this DBIF (2008); Hartig12 Q. borealis var. and stems; dorsalis robur) species Williams maxima mature in Torymus affinis IT N/A 0.4 (2010); Askew Sexual generation Q. cerris September Torymus auratus GB 5.9-14.7 et al. (2013); Q. faginea Torymus flavipes GB (Q. None Ellis (2018) Q. frainetto Adults emerge robur) observed Q. pubescens March to August Ormyrus pomaceus IT N/A 0.6 of 2nd year Ormyrus spp. IT N/A 0.2 Megastigmus GB/IT None 1.2 dorsalis observed Hobbya stenonota IT N/A 0.2 Mesopolobus GB None albitarsus? observed Mesopolobus N/A fuscipes Mesopolobus tibialis N/A Eupelmus azureus IT N/A 0.4 Eupelmus kiefferi IT N/A 0.4 Eupelmus urozonus IT N/A 0.6 Eupelmus spp. IT N/A 0.6 Aulogymnus GB (Q. 5.9-14.7 0.6 arsames robur)/IT Aulogymnus spp. IT N/A 0.2 Aprostocetus sp. N/A Total ER = 5.9 Inquilines: Saphonecrus N/A conatus Synergus apicalis N/A Synergus GB (Q. 5.9-14.7 crassicornis robur) Synergus pallipes N/A Synergus tibialis N/A Q. petraea Sycophila iracemae N/A

12 Ferracini et al. (2017) report that galls of the sexual generation of A. curvator are attacked by T. sinensis in the field (see Table 3 for further details).

Parasitism levels in oak galls 28

Andricus inflator Globular Q. robur Galls found Rare and Eurytoma GB (Q. 10 No data 5.9 Redfern et al. Hartig13 Gall September to scattered (local) brunniventris robur)/IT available (2002); BRC- Q. borealis var. December on Torymus auratus N/A for this DBIF (2008); Asexual generation maxima vegetative buds; Ormyrus pomaceus N/A species Williams (= globuli) Q. faginea mature end of Mesopolobus GB (Q. 10 11.8 (2010); Askew Q. frainetto October sericeus robur)/IT et al. (2013); Q. lusitanica Eupelmus N/A Ellis (2018) Q. pubescens spongipartus Q. rubra Eupelmus urozonus N/A Total ER = 17.6 Inquilines: Saphonecrus N/A connatus

Synergus apicalis N/A Synergus N/A crassicornis Synergus hayneanus N/A Synergus N/A pallidipennis Synergus pallipes N/A Synergus radiatus N/A Synergus ruficornis GB None observed Synergus tibialis N/A Synergus N/A umbraculus Andricus kollari Q. cerris Galls found Common Mesopolobus dubius GB None None No data Redfern et al. Hartig14 Q. x hispanica March to June on observed observed available (2002); Stone buds; mature end Mesopolobus GB (Q. >20.8 4.75 – 57 for this et al., (2002); Sexual generation of March fuscipes cerris) (33.79) species BRC-DBIF (= circulans) Mesopolobus tibialis GB (Q. 1 0 -8.25 (2008); cerris) (1.38) Williams

13 Williams (2010) states that the asexual generation of A. inflator is quite common. 14 Andricus kollari is an invasive species that came across with Q. cerris. It is thought that the sexual generation can be permanently skipped because this gall causer occurs in regions where Q. cerris does not exist. Schönrogge et al. (1998) report that 4 - 70% of galls were parasitized in their 1994/1995 study.

Parasitism levels in oak galls 29

Adults emerge Mesopolobus GB (Q. 1 0 – 12.5 (2010); Askew March to June xanthocerus cerris) (1.89) et al. (2013); Aulogymnus N/A N/A Ellis (2018) gallarum Aulogymnus N/A N/A testaceoviridis Mean total ER = 37.1 Inquilines: Ceroptres cerri Andricus kollari Marble Q. petraea Galls found June Very common Eurytoma adleriae IT N/A N/A Redfern et al. 15 Hartig Gall Q. robur onwards in buds; Eurytoma GB (Q. 4.7 – 14.8 2.5 – 20 6.5 (2002); Stone matures end of brunniventris robur)/IT (11.25) et al., (2002); Asexual generation Q. borealis September (Q. BRC-DBIF Q. canariensis pubescens) (2008); Q. frainetto Adults emerge Williams Q. x hispanica August to Eurytoma pistaciae IT N/A N/A 0.3 (2010); st Q. ilex October in 1 Eurytoma setigera N/A N/A Schönrogge et Q. infectoria year, March to Sycophila biguttata GB (Q. 0.6 None 0.7 al. (2012); nd Q. lusitanica September in 2 robur)/IT observed Askew et al. Q. mongolica year, and (2013); Ellis Sycophila flavicollis GB None None Q. pontica emergence can (2018) observed observed Q. pubescens also occur in Sycophila variegata GB (Q. 0.6 None Q. pyrenaica subsequent years robur) observed Q. rotundifolia Megastigmus GB (Q. 4.7 – 14.8 None 2.3 Q. suber dorsalis robur)/IT observed Q. trojana Megastigmus GB (Q. 1.2 - 3 None 2.0 stigmatizans robur)/IT observed (Q. pubescens) Torymus affinis IT N/A N/A 0.1 Torymus auratus GB (Q. None 37.2 – 180 15.4 robur)/IT observed (108.6) Torymus GB 10.7 - None auratus/cingulatus 35.5 observed

15 Askew et al. (2013) suggest that much of the literature recording Eupelmus annulatus are misidentification of E. spongipartus. Askew et al. (2013) report a percentage representation of inquilines of 34% for asexual generation galls.

Parasitism levels in oak galls 30

Torymus ?erucarum N/A N/A Torymus geranii GB (Q. None None robur) observed observed Torymus spp. GB (Q. 10 – 25.5 (males) robur) (17.75) Ormyrus nitidulus GB (Q. None None 1.4 robur)/IT observed observed (Q. robur) Ormyrus pomaceus N/A N/A Ormryus spp. IT 1.7 Caenacis lauta GB (Q. 0.6 None robur) observed Cecidostiba fungosa GB (Q. None 0 – 20 (10) 0.4 robur)/IT observed Cecidostiba N/A N/A geganius Cecidostiba GB (Q. None None semifascia robur) observed observed Cecidostiba GB (Q. None None semifationis robur) observed observed Cyrtoptyx robustus IT N/A N/A Hobbya stenonota GB (Q. 3.6 – 11.8 None 1.0 robur)/IT observed Mesopolobus GB (Q. 0.6 None amaenus robur) observed Mesopolobus dubius GB None None observed observed Mesopolobus GB (Q. None None fasciiventris (Q. robur) observed observed robur) Mesopolobus GB None None fuscipes observed observed Mesopolobus GB (Q. 4.1 – 12.4 None 0.3 sericeus robur)/IT observed Mesopolobus tibialis GB (Q. None None robur) observed observed Mesopolobus GB None None xanthocerus observed observed

Parasitism levels in oak galls 31

Eupelmus annulatus GB None None observed observed Eupelmus azureus IT N/A N/A 4.5 Eupelmus kiefferi IT N/A N/A 0.3 Eupelmus GB None None spongipartus observed observed Eupelmus urozonus GB (Q. 1.2 0 – 1 (0.5) 0.3 robur)/IT Eupelmus vesicularis N/A N/A Eupelmus spp. IT 0.1 Aulogymnus N/A N/A ?arsames Aulogymnus N/A N/A gallarum Aulogymnus IT N/A N/A 0.1 skianeuros Aulogymnus GB (Q. None None trilineatus robur) observed observed Baryscapus N/A N/A ?anasillus Baryscapus N/A N/A berhidanus Baryscapus N/A N/A ?pallidae (Scambus sp.) N/A N/A Mean total Total ER ER = 148.1 = 37.5 Inquilines:

Ceroptres clavicornis GB 2.4 – 5.9 None observed Saphonecrus GB None None connatus observed observed Synergus GB (Q. None None crassicornis robur)/IT observed observed (Q. pubescens) Synergus facialis GB (Q. 1.2 - 3 0 – 15a robur)/IT (7.5)

Parasitism levels in oak galls 32

(Q. pubescens) Synergus hayneanus N/A N/A Synergus incrassatus N/A N/A Synergus pallicornis GB None None observed observed Synergus GB None None pallidipennis observed observed Synergus pallipes GB (Q. None None robur) observed observed Synergus radiatus N/A N/A Synergus reinhardi GB (Q. >11.8 0 – 95 robur) (47.5) Synergus N/A N/A thaumacerus Synergus tibialis N/A N/A Synergus GB (Q. 1.8 – 3.6 20 – 95 umbraculus robur)/IT (57.5) Mean total IR = 112.5 Andricus legitimus Stunted Q. petraea Galls found May Uncommon (but Eurytoma No data No data No data Redfern et al. Wiebes-Rijks16 Acorn Gall Q. robur to September difficult to spot) brunniventris available available available (2002); BRC- onwards on , Megastigmus for this for this for this DBIF (2008); Asexual generation Q. faginea mature end of dorsalis species species species Williams Q. pubescens September Hobbya stenonota (2010); Askew Q. pyrenaica Mesopolobus tibialis et al. (2013); Adults emerge Eupelmus Ellis (2018) April to May and spongipartus September three to four years Inquilines: later Synergus GB (Q. clandestinus robur) Synergus GB crassicornis Synergus facialis

16 Redfern et al. (2002) suggests that A. legitimus is common. Only the asexual generation is known.

Parasitism levels in oak galls 33

Andricus lignicola Q. cerris Galls found April Common and Mesopolobus dubius GB (Q. No data 0 – 1.7 (0.6) No data Redfern et al. (Hartig)17 to May on widespread cerris) available available (2002); Stone vegetative buds; Mesopolobus GB (Q. for this 4.4 – 50a for this et al., (2002); (= A. lignicolus) mature March fuscipes cerris) species (24.3) species BRC-DBIF onwards Mesopolobus tibialis GB (Q. 0 – 2.4 (0.6) (2008); Sexual generation cerris) Williams (= vanherni) Adults emerge Mesopolobus GB (Q. 0 – 4 (0.6) (2010); Askew September of 1st xanthocerus cerris) et al. (2013); year and March Aulogymnus GB None Ellis (2018) to June of 2nd skianeuros observed year Mean total ER = 26.1 No known inquilines Andricus lignicola Cola-Nut Q. petraea Galls found July Common Eurytoma adleriae No data N/A Redfern et al. (Hartig)18 Gall Q. robur to October on Eurytoma GB (Q. available None 1.0 (2002); Stone vegetative buds; brunniventris robur)/IT for this observed et al., (2002); (= A. lignicolus) Q. cerris mature in Eurytoma setigera species N/A BRC-DBIF Q. frainetto October Sycophila biguttata GB/IT None 0.1 (2008); Asexual generation Q. mongolica observed Williams Q. montana Adults emerge Sycophila variegata N/A (2010); Askew Q. phellos November to Megastigmus GB (Q. None 4.6 et al. (2013); Q. pubescens December of 1st dorsalis robur)/IT observed Ellis (2018) Q. pyrenaica year and April to Megastigmus GB None nd July of 2 year stigmatizans observed Torymus auratus GB (Q. None 1.4 robur)/IT observed Torymus geranii GB None observed Torymus spp. None (males) observed (Perilampus N/A ruficornis) Ormyrus nitidulus GB/IT None 18.0 observed

17 Andricus lignicola is an invasive species which came across with Q. cerris. Schonrogge et al. (1998) report that 0 – 46% of galls were parasitized in their 1994/1995 study. 18 Andricus lignicola is an invasive species which came across with Q. cerris. Askew et al. (2013) report a percentage representation of inquilines of 35% for asexual generation galls. Ferracini et al. (2017) report that galls of the asexual generation of A. lignicola are attacked by T. sinensis in the field (see Table 3 for further details).

Parasitism levels in oak galls 34

Ormyrus pomaceus N/A Orymrus spp. 1.0 Caenacis lauta N/A Cecidostiba fungosa IT N/A 0.2 Cecidostiba N/A semifacia Cecidostiba GB None semifationis observed Eumacepolus sp.? N/A Mesopolobus GB (Q. None 0.1 amaenus robur)/IT observed Mesopolobus dubius N/A Mesopolobus GB (Q. None fasciiventris robur) observed Mesopolobus None fuscipes observed Mesopolobus GB (Q. None 1.0 sericeus robur)/IT observed

Mesopolobus tibialis N/A Mesopolobus GB None xanthocerus observed Eupelmus azureus IT N/A 0.1 Eupelmus N/A spongipartus

Eupelmus urozonus GB (Q. None robur) observed Reikosiella rostrata N/A Aulogymnus GB None skianeuros observed Aulogymnus N/A trilineatus Aprostocetus N/A aethiops Mean total Total ER ER = 0.0 = 12.7 Inquilines:

Parasitism levels in oak galls 35

Ceroptres clavicornis GB None observed Saphonecrus GB None connatus observed Synergus apicalis GB None observed Synergus GB None crassicornis observed Synergus facialis GB (Q. 0 – 50 (7.4) robur) Synergus hayneanus N/A Synergus pallicornis N/A Synergus GB None pallidipennis observed Synergus pallipes GB None observed Synergus reinhardi GB (Q. 0 – 7.5 (1.1) robur) Synergus ruficornis N/A Synergus GB (Q. 0 – 0.7 (0.1) umbraculus robur) Mean total IR = 8.6 Andricus lucidus Q. petraea? Galls found on Rare Eurytoma No data No data Redfern et al. (Hartig)19 Q. robur? flowers in late brunniventris available available (2002); Stone Q. cerris Spring; mature in Eurytoma setigera for this for this et al., (2002); Sexual generation September Sycophila biguttata GB/IT species species 400 BRC-DBIF (= aestivalis) Q. frainetto Sycophila variegata IT 12.5 (2008); Q. pubescens Adults emerge Torymus auratus GB Williams Q. suber September of 1st Ormyrus nitidulus (2010); year and Ormyrus pomaceus Schönrogge et February to Cecidostiba fungosa al. (2012); nd March of 2 year Hobbya stenonota Askew et al. (2013); Ellis Mesopolobus xanthocerus (2018)

19 Andricus lucidus is an invasive species which came across with Q. cerris. It was discovered in Great Britain in 2000. BRC-DBIF (2008) list Q. petraea and Q. robur as hosts but other sources do not include these two species of oak.

Parasitism levels in oak galls 36

Eupelmus spongipartus Eupelmus urozonus GB Aulogymnus gallarum Baryscapus sp. Total ER = 412.5 Inquilines: Synergus pallipes Synergus umbraculus Andricus lucidus Hedgehog Q. petraea Galls on buds and Rare (south east: Eurytoma adleriae No data No data Redfern et al. (Hartig)20 Gall or Q. robur acorns; mature Maidenhead, available available (2002); Stone Bristly July onwards Ascot area, Eurytoma GB/IT for this for this 22.1 et al., (2002); Asexual generation Gall Q. frainetto Regent’s Park, brunniventris species species BRC-DBIF Q. infectoria Adults emerge Hampstead (2008); subsp. veneris January to April Heath, Eurytoma pistaciae IT 4.6 Williams Q. lusitanica of 2nd year Berkshire) Eurytoma setigera (2010); Askew Q. pubescens et al. (2013); Q. pyrenaica Sycophila biguttata GB/IT 32.3 Ellis (2018) Sycophila variegata IT 6.7 Megastigmus IT 56.1 dorsalis Megastigmus IT 11.0 stigmatizans Torymus auratus GB/IT 0.3 Torymus cyaneus Torymus flavipes IT 0.3 Ormyrus nitidulis IT 4.3 Ormyrus pomaceus IT 3.4 Ormyrus spp. IT 13.9 Cauenacis lauta Cecidostiba fungosa GB/IT 17.8

20 Andricus lucidus is an invasive species which came across with Q. cerris. It was discovered in Great Britain in the 1990s. Askew et al. (2013) report a percentage representation of inquilines of 36% for asexual generation galls. Ferracini et al. (2017) report that galls of the asexual generation of A. lignicola are attacked by T. sinensis in the field (see Table 3 for further details).

Parasitism levels in oak galls 37

Cecidostiba IT 0.1 semifascia

Hobbya stenonota IT 1.6

Mesopolobus IT 0.8 amaenus Mesopolobus GB/IT 0.8 sericeus Mesopolobus tibialis IT 7.3 Mesopolobus GB/IT 0.1 xanthocerus Mesopolobus spp. IT 0.1 Euepelmus azureus IT 5.5 Eupelmus kiefferi IT 0.1 Eupelmus sponipartus Eupelmus urozonus GB/IT 3.0

Eupelmus spp. IT 0.1 Aulogymnus IT 0.1 arsames

Aulogymnus IT 0.1 gallarum

Aulogymnus IT 0.6 trilineatus Aulogymnus spp. IT 0.2 Baryscapus ?anasillus Baryscapus berhidanus Baryscapus spp. IT 2.6 (Scambus elegans) Total ER = 189.1 Inquilines:

Parasitism levels in oak galls 38

Ceroptres clavicornis GB Synergus facialis Synergus hayneanus Synergus pallidipennis Synergus pallipes Synergus GB umbraculus Andricus nudus (= Bald-Seed Q. petraea Galls found May Rare and Ormocerus latus No No data No data No data Redfern et al. A. malpighii) Adler Gall Q. robur to June on scattered parasitoids available available available (2002); BRC- flowers; mature Mesopolobus tibialis or for this for this for this DBIF (2008); Sexual generation Q. faginea end of May inquilines species species species Williams Q. pyrenaica Mesopolobus known to (2010); Askew Adults emerge xanthocerus be et al. (2013); May to June associated Ellis (2018) Inquilines: in the UK Synergus facialis Synergus pallipes Synergus radiatus Andricus nudus (= Malpighi’s Q. petraea Galls found Rare Eurytoma No data No data No data Redfern et al. A. malpighii) Adler Gall Q. robur September to brunniventris available available available (2002); October on Mesopolobus for this for this for this Williams Asexual generation Q. faginea shoots and fasciiventris species species species (2010); BRC- Q. lusitanica vegetative buds; Mesopolobus DBIF (2008); Q. pubescens mature end of serceus Askew et al. Q. pyrenaica September Mesopolobus tibialis (2013); Ellis Pteromalus sp. (2018) Adults emerge Eupelmus urozonus st October of 1 year and March Inquilines: nd to April of 2 Saphonecrus year connatus Synergus facialis Synergus pallipes GB Synergus radiatus Synergus thaumacerus Q. petraea Not present? Mesopolobus tibialis

Parasitism levels in oak galls 39

Andricus Q. robur No known inquilines BRC-DBIF quadrilineatus (2008); Askew Hartig21 Q. pubescens et al. (2013); Ellis (2018) Sexual generation Andricus Furrowed- Q. petraea Galls found May Common Eurytoma N/A N/A No data Redfern et al. quadrilineatus Catkin Q. robur to June onwards brunniventris available (2002); BRC- Hartig Gall on the flowers Eurytoma N/A N/A for this DBIF (2008); Q. pubescens and leaves; querceticola species Williams Asexual generation mature end of Sycophila biguttata N/A N/A (2010); Askew (= marginalis) June Torymus auratus GB 0.8 -2.0 None et al. (2013); observed Ellis (2018) Adults emerge Torymus flavipes GB (Q. None None February to April robur) observed observed of the 2nd year Ormyrus pomaceus N/A N/A Ormocerus latus N/A N/A Caenacis lauta N/A N/A Mesopolobus GB None 6.9 (6.9) amaenus observed Mesopolobus N/A N/A fasciiventris Mesopolobus GB None 35.9 (35.9) sericeus observed Mesopolobus tibialis N/A N/A Mesopolobus GB (Q. 0.8 None xanthocerus robur) observed Eupelmus urozonus N/A N/A Aulogymnus GB (Q. 0.4 None arsames robur) observed Aulogymnus GB (Q. >8.1 None euedoreschus robur) observed Aulogymnus GB (Q. None None gallarum robur) observed observed Aulogymnus N/A N/A tetaceoviridis

21 Sexual generations of A. quadrilineatus are regularly skipped; Williams (2010) does not list the sexual generation in Great Britain and Redfern et al. (2002) state that the sexual generation is not known.

Parasitism levels in oak galls 40

Aulogymnus N/A N/A trilineatus (‘Hemiteles’ sp.) GB (Q. 0.4 None robur) observed Mean total ER = 42.8 Inquilines: Ceroptres clavicornis Synergus facialis 1.6 – 4.1 36 (36) Synergus pallicornis Synergus pallipes 3.7 – 10.7 41 (41) Synergus radiatus None None observed observed Mean total IR = 77 Andricus Q. cerris Galls found April Common Sycophila biguttata GB (Q. No data None No data Redfern et al. quercuscalicis Q. suber to June on cerris) available observed available (2002); Stone (Burgsdorf)22 flowers; mature Megastigmus GB (Q. for this None for this et al., (2002); early April dorsalis cerris) species observed species BRC-DBIF Sexual generation onwards Torymus flavipes N/A (2008); (= cerri) Ormyrus pomaceus GB (Q. None Williams Adults emerge cerris) observed (2010); Askew April to June Ormocerus vernalis GB (Q. None et al. (2013); cerris) observed Ellis (2018) Cecidostiba fungosa GB (Q. None cerris) observed Mesopolobus GB (Q. None amaenus cerris) observed Mesopolobus dubius GB (Q. 0.96 – 1.7 cerris) (1.2) Mesopolobus GB (Q. 2.5 – 33 fuscipes cerris) (16.1) Mesopolobus GB N/A ?mediterraneus

22 is an invasive species which came across with Q. cerris. Askew et al. (2013) report a percentage representation of inquilines of 0.08% for sexual generation galls. Stone et al. (2002) report 20 - 45% mortality of these galls due to parasitoid attack and Schonrogge et al. (1998) report that 10 – 45% galls were parasitized in their 1994/1995 study.

Parasitism levels in oak galls 41

Mesopolobus GB (Q. None sericeus cerris) observed Mesopolobus tibialis GB (Q. 0 – 3.8 (1.1) cerris) Mesopolobus GB (Q. 0.3 – 10 xanthocerus cerris) (4.6) Eupelmus urozonus GB (Q. None cerris) observed Aulogymnus N/A gallarum Aulogymnus N/A obscuripes Aulogymnus N/A testaceoviridis Aprostocetus GB None aethiops observed Aprostocetus N/A cerricola Aprostocetus nr N/A viridinitens Pediobius clita GB None observed Mean total ER = 22.94 Inquilines: Synergus tibialis N/A Synergus N/A umbraculus Andricus Knopper Q. petraea Galls found May Introduced into Eurytoma adleriae No data N/A No data Redfern et al. quercuscalicis oak gall Q. robur to October on the British Isles Eurytoma GB/IT available 0 – 50 available (2002); Stone (Burgsdorf)23 and seeds; in the 1960s brunniventris (24.4) et al., (2002);

23 Andricus quercuscalicis is an invasive species which came across with Q. cerris. Parasitism was low until 1990 but is now increasing and Ellis (2004) reports 17 - 31.5% of galls are attacked by parasitoids. Attack mirrors the spread of the gall, so numbers are increasing with time, and are spreading further north with time (Schönrogge et al., 1995). Synergus facialis is the most common Synergus spp. Inquiline attack rates in the south-east of England now exceed 1.0 per gall (Ellis, 2004). Askew et al. (2013) report a percentage representation of inquilines of 40% for asexual generation galls. Further detailed information on levels of parasitism in this species can be found in Schönrogge et al. (1996), Ellis (2005) and Ellis (2006).

Parasitism levels in oak galls 42

Q. x hynaldiana mature in Sycophila biguttata GB (Q. for this 0 – 4.75 for this BRC-DBIF Asexual generation Q. macrolepis September Very common robur)/IT species (1.4) species (2008); Q. pubescens and widespread Sycophila variegata N/A Williams Q. pyrenaica Adults can throughout Megastigmus GB/IT 0 – 40 (10) (2010); Askew Q. x turneri emerge October England and dorsalis et al. (2013); to December in Wales. Megastigmus GB (Q. None Ellis (2018); 1st year but more stigmatizans robur)/IT observed NatureSpot usually January Torymus auratus GB (Q. None (2019) to April of 2nd robur) observed year Torymus cyaneus GB None observed Torymus geranii GB (Q. 0 – 0.5 (0.1) robur) Torymus spp. 0 – 4.5 (2.9) (males) Ormyrus nitidulus GB (Q. 0 – 1 (0.3) robur)/IT Ormyrus pomaceus IT N/A Arthrolytus ocellus GB (Q. None robur) observed Cecidostiba fungosa GB (Q. 0 – 300 (75) robur)/IT Cecidostiba GB (Q. None semifascia robur) observed Cecidostiba GB None semifationis observed Hobbya stenonata N/A Mesopolobus GB (Q. 0 – 1.5a amaenus robur) (0.9) Mesopolobus N/A fasciiventris Mesopolobus GB (Q. 0.67a – 95 sericeus robur) (44.8) Mesopolobus tibialis GB (Q. 0 – 4 (1.0) robur) Eupelmus N/A spongipartus Eupelmus urozonus GB (Q. 0 – 20 (7.1) robur)/IT

Parasitism levels in oak galls 43

Eupelmus vesicularis GB (Q. None robur) observed Aulogymnus N/A gallarum Aulogymnus N/A skianeuros Aulogymnus IT N/A trilineatus Baryscapus N/A ?anasillus Baryscapus IT N/A berhidanus Baryscapus N/A ?pallidae spp. IT N/A Mastrus castaneus GB (Q. None robur) observed Gelis formicarius GB None observed Spilomicrus GB None stigmaticalis observed Mean total ER = 169.4 Inquilines: Ceroptres clavicornis N/A Saphonecrus haimi N/A Synergus apicalis N/A Synergus N/A crassicornis Synergus facialis GB (Q. 1.2 – 352 robur)/IT (173.8) Synergus hayneanus N/A Synergus incrassatus N/A Synergus pallicornis GB None observed Synergus N/A pallidipennis Synergus pallipes GB (Q. 0 – 5 (1.3) robur)

Parasitism levels in oak galls 44

Synergus radiatus GB None observed Synergus reinhardi IT N/A Synergus N/A thaumacerus Synergus GB (Q. None umbraculus robur)/IT observed Mean total IR = 175.1 Andricus The Bud Q. petraea Galls found June Rare and No known No data No data No data Redfern et al. quercuscorticis (L.) Gall Q. robur to July on scattered parasitoids available available available (2002); BRC- vegetative buds, for this for this for this DBIF (2008); Sexual generation Q. cerris shoots and Inquilines: species species species Williams (= gemmatus) Q. lusitanica stems; mature in Synergus incrassatus GB (2010); Ellis Q. pubescens June (2018) Q. pyrenaica Adults emerge in June Andricus Bark-Gall Q. petraea Galls found any Rare and Eurytoma N/A No data No data Redfern et al. quercuscorticis Q. robur time of the year scattered - brunniventris available available (2002); BRC- (L.)24 on stems and widespread, Torymus formosus N/A for this for this DBIF (2008); Q. lusitanica trunks; mature in possibly locally Torymus nobilis N/A species species Williams Asexual generation Q. pubescens May frequent (likely Torymus pleuralis N/A (2010); Askew Q. pyrenaica to be under et al. (2013); Adults emerge recorded) Inquilines: Ellis (2018); April to July Synergus facialis GB (Q. None NatureSpot robur) observed (2019) Synergus incrassatus GB None observed Andricus Knot Gall Q. petraea Galls found June Common Eurytoma No No data No data Redfern et al. quercusradicis (F.)25 Q. robur to August on bruniiventris parasitoid available available (2002); BRC-

24 Niblett (1944) reports infestation rates for S. incrassatus on asexual generation A. quercuscorticis ranging from 3.7 - 15% at two locations in the south of England. In addition, at a further location the author reports emergence of S. incrassatus and parasitoids (Torymidae, Eurytomidae and Pteromalidae) from the galls but does not provide the number of galls examined to enable calculation of ER and IR. 25 Askew et al. (2013) report a percentage representation of inquilines of 45% for sexual generation galls. Niblett (1944) report emergence of Synergus species (possible S. apicalis) from the sexual generation of A. quercusradicis but does not indicate the numbers that emerged.

Parasitism levels in oak galls 45

shoots, leaves Sycophila flavicollis GB (Q. or for this for this DBIF (2008); Sexual generation Q. cerris and stems; robur) inquiline species species Williams (= trilineata) Q. coccifera mature in July Sycophila variegata GB (?Q. attack (2010); Askew Q. faginea robur) observed et al. (2013); Q. frainetto Adults emerge Megastigmus GB (Q. for this Ellis (2018) Q. lusitanica July to November dorsalis robur) species Q. pubescens Ormyrus pomaceus GB (?Q. Q. pyrenaica robur) Q. suber Arthrolytus incises Arthrolytus nanus Cecidostiba fungosa Eumacepolus obscurior Hobbya stenonota Mesopolobus GB (Q. amaenus robur) Mesopolobus dubius Mesopolobus mediterraneus Mesopolobus GB (Q. sericeus robur) Mesopolobus tarsatus Eupelmus aseculatus Eupelmus urozonus Eupelmus vesicularis Tetrastichinae sp.

Inquilines: Ceroptres clavicornis GB Saphonecrus GB (Q. connatus robur) Synergus apicalis GB (Q. robur) Synergus facialis GB (Q. robur) Synergus incrassatus GB Synergus GB rotundiventris

Parasitism levels in oak galls 46

Synergus tibialis GB Andricus Truffle Q. petraea Galls found in Eurytoma adleriae N/A No data No data Redfern et al. quercusradicis (F.)26 gall Q. robur September on Eurytoma N/A available available (2002); BRC- and stems; brunniventris for this for this DBIF (2008); Asexual generation Q. canariensis mature in August Torymus erucarum GB (Q. None species species Williams Q. coccifera of 2nd year robur & Q. observed (2010); Askew Q. faginea petraea) et al. (2013); Q. lusitanica Adults emerge Torymus flavipes GB None Ellis (2018) Q. pubescens March to April of observed Q. pyrenaica 3rd Spring Torymus formosus GB (Q. None Q. suber robur) observed Torymus geranii GB None observed Torymus nobilis GB (Q. None robur) observed Torymus scutellaris GB (Q. None robur) observed Torymus sp. 33.3 Ormyrus nitidulus N/A Caenacis lauta GB None observed Cecidostiba GB (Q. 33.3 geganius robur) Mesopolobus GB None sericeus observed Eupelmus N/A spongipartus Eupelmus vesicularis N/A

Inquilines: Synergus facialis GB None observed Synergus incrassatus GB 33.3 Synergus tibialis N/A

26 Askew et al. (2013) report a percentage representation of inquilines of 13% for asexual generation galls. Niblett (1944) provides some information for A. quercusradicis but does not indicate the generation. From the dates of emergence that he provides for the gall former, it is likely that some of the information pertains to the asexual generation: 143 Torymidae are reported as emerged from one gall; 7 Torymidae/Pteromalidae + an unstated number of S. incrassatus were reported from a second gall.

Parasitism levels in oak galls 47

Andricus Cotton- Q. petraea Galls found May Rare and Eurytoma adleriae N/A N/A No data Redfern et al. quercusramuli (L.)27 Wool gall Q. robur to June on scattered Eurytoma N/A N/A available (2002); BRC- flowers; matures (probably under brunniventris for this DBIF (2008); Sexual generation Q. cerris in June recorded) Sycophila biguttata GB (Q. None None species Williams Q. dalechampii robur) observed observed (2010); Askew Q. faginea Adults emerge Megastigmus N/A N/A et al. (2013); Q. frainetto May to August dorsalis Ellis (2018); Q. hartwissiana Torymus auratus 25 None NatureSpot Q. lusitanica observed (2019) Q. pubescens Torymus flavipes GB (Q. None 44 (44) Q. pyrenaica robur) observed Torymus geranii N/A N/A Torymus spp. None 22 (22) (males) observed Ormyrus pomaceus N/A N/A Ormocerus latus N/A N/A Ormocerus vernalis N/A N/A Cecidostiba fungosa GB None 10 (10) observed Cecidostiba N/A N/A semifascia Hobbya stenonota N/A N/A Mesopolobus N/A N/A albitarsus Mesopolobus N/A N/A amaenus Mesopolobus dubius N/A N/A Mesopolobus N/A N/A fasciiventris Mesopolobus GB None 444a (444) fuscipes observed Mesopolobus N/A N/A mediterraneus Mesopolobus tibialis None 75.6 (75.6) observed

27 Askew et al. (2013) report a percentage representation of inquilines of 0.5% for sexual generation galls.

Parasitism levels in oak galls 48

Mesopolobus GB None 27.8 (27.8) xanthocerus observed Eupelmus N/A N/A spongipartus Eupelmus urozonus N/A N/A Aulogymnus N/A N/A arsames Aulogymnus GB 150 - 500 None gallarum (Q. robur) observed Aulogymnus GB None None skianeuros observed observed Aulogymnus N/A N/A testaceoviridis Aprostocetus N/A N/A aethiops Aprostocetus N/A N/A domenichinii Mean total ER = 623.4 Inquilines: Ceroptres clavicornis GB None None observed observed Saphonecrus N/A N/A connatus Synergus facialis GB None None observed observed Synergus pallipes N/A N/A Synergus radiatus N/A N/A Andricus The Q. petraea Galls found: Rare and Mesopolobus GB (Q. No data No data No data Redfern et al. quercusramuli (L.) Autumn- Q. robur September to scattered (highly sericeus robur) available available available (2002); BRC- Gall October on localised) for this for this for this DBIF (2008); Asexual generation Q. pubescens shoots and Inquilines: species species species Williams (= autumnalis) vegetative buds; Saphonecrus (2010); Askew mature mid- connatus et al. (2013); October Synergus facialis Ellis (2018); Synergus pallipes NatureSpot Adults emerge Synergus radiatus (2019) March to June of Synergus tibialis GB 2nd year

Parasitism levels in oak galls 49

Andricus rhizomae Q. petraea Galls on leaves No information No information BRC-DBIF (= A. rhyzomae) Q. robur available available (2008) (Hartig)28 Adults emerge in August

Sexual generation Andricus rhizomae Q. petraea Galls found Very rare and Torymus nobilis No No data No data No data Redfern et al. (= A. rhyzomae) Q. robur January to scattered parasitoids available available available (2002); BRC- (Hartig) December on Inquilines: or for this for this for this DBIF (2008); Q. lusitanica bark (roots, Synergus incrassatus inquilines species species species Williams Asexual generation Q. pubescens shoots and Synergus known to (2010); Askew (= nodifex) Q. pyrenaica stems); mature in subterraneus be et al. (2013); September associated Ellis (2018) in the UK Adults emerge February to April Andricus Spindle- Q. petraea Galls found April Rare Eurytoma N/A No data Redfern et al. seminationis Gall or Q. robur to June on brunniventris available (2002); BRC- (Giraud)29 Barley- flowers and Torymus auratus GB 5.9 for this DBIF (2008); Corn Gall Q. pubescens (rarely) leaves; Torymus flavipes GB None species Williams Asexual generation mature end of observed (2010); Askew June Ormyrus pomaceus N/A et al. (2013); Mesopolobus GB None Ellis (2018) Adults emerge sericeus observed March to May of Eupelmus N/A 2nd year spongipartus Aprostocetus GB None aethiops observed

Inquilines: Ceroptres clavicornis N/A Synergis facialis GB None observed Synergus incrassatus N/A

28 The sexual generation of A. rhizomae is not listed in Williams (2010) or Askew et al. (2013). Ellis (2018) states that it is assumed that A. rhizomae is the sexual generation of A. testaceipes but experimental proof of this is still needed. 29 Only the asexual generation of A. seminationis is known.

Parasitism levels in oak galls 50

Synergus pallipes GB None observed Synergus GB 47 - 147 facialis/pallipes Synergus radiatus GB None observed Andricus solitarius Q. petraea Galls found in Common Torymus flavipes GB None No data No data Redfern et al. (Fonscolombe) Q. robur April on flowers; observed available available (2002); BRC- mature in April Mesopolobus N/A for this for this DBIF (2008); Sexual generation Q. cerris fuscipes species species Williams (= occultus) Q. pubescens Adults emerge in Mesopolobus N/A (2010); Askew Q. pyrenaica April mediterraneus et al. (2013); Mesopolobus tibialis N/A Ellis (2018) Mesopolobus N/A xanthocerus

No known inquilines Andricus solitarius Hairy- Q. petraea Galls found June Common Eurytoma GB (Q. 9.7 - 17 No data 1.2 Redfern et al. (Fonscolombe) Spindle Q. robur to September on brunniventris robur)/IT available (2002); BRC- Gall shoots and Eurytoma pistaciae IT N/A for this 1.8 DBIF (2008); Asexual generation Q. canariensis vegetative buds; Eurytoma setigera N/A species Williams Q. frainetto mature end of Sycophila biguttata IT N/A 1.2 (2010); Askew Q. ilex August Sycophila variegata N/A et al. (2013); Q. infectoria Megastigmus N/A Ellis (2018) subsp. veneris Adults emerge dorsalis Q. lusitanica August to Ormyrus pomaceus IT N/A 1.8 Q. pubescens September Cecidostiba fungosa N/A Q. pyrenaica Hobbya stenonota N/A Q. suber Mesopolobus GB (Q. 2.4 amaenus robur) Mesopolobus GB (Q. 2.4 0.6 sericeus robur)/IT Mesopolobus tibialis N/A Mesopolobus N/A xanthocerus Eupelmus azureus IT N/A 2.4 Eupelmus N/A spongipartus

Parasitism levels in oak galls 51

Eupelmus urozonus GB (Q. None 1.2 robur)/IT observed Aulogymnus N/A gallarum Aulogymnus IT (Q. N/A trilineatus petraea & Q. pubescens) Total ER = 10.3 Inquilines: Ceroptres clavicornis N/A Synergus facialis GB None observed Synergus pallipes GB None observed Synergus radiatus GB (Q. None robur) observed Synergus tibialis GB None observed Synergus sp. 19.5 - 61 Andricus sufflator Q. petraea Galls found in Rare and Mesopolobus No data No data No data BRC-DBIF Mayr30 June on leaves scattered amaenus available available available (2008); Askew Q. pubescens Mesopolobus for this for this for this et al. (2013); Sexual generation Q. frainetto lichtensteini species species species Ellis (2018) (= A. Q. lusitanica Eupelmus urozonus gallaeurnaeformis?) Q. pyrenaica Aulogymnus gallarum

Inquilines: Synergus IT thaumacerus Andricus Leaf-Vein Q. petraea Galls found July Rare Mesopolobus sp. GB 12.5 No data No data BRC-DBIF testaceipes Hartig Gall Q. robur to September on available available (2008); shoots and Inquilines: Williams

30 The sexual generation of A. sufflator is listed on the BRC-DBIF (2008) but not listed by Redfern et al. (2002) or Williams (2010). Ellis (2018) suggests that A. sufflator is the sexual generation of A. gallaeurnaeformis. The parasitoids/inquilines listed are as for A. gallaeurnaeformis sexual generation (Askew et al., 2013).

Parasitism levels in oak galls 52

Sexual generation Q. cerris leaves; mature Synergus sp. GB 37.5 - 75 for this for this (2010); Askew Q. ilex end of August species species et al. (2013); Q. lusitanica Ellis (2018) Q. pubescens Adults emerge Q. pyrenaica August to Q. suber September Andricus Red- Q. petraea Galls found in Locally common Eurytoma GB 2 No data 10.8 Redfern et al. testaceipes (Hartig) Barnacle Q. robur September on brunniventris available (2002); BRC- Gall shoots and Torymus erucarum N/A for this DBIF (2008); Asexual generation stems; mature in Torymus formosus N/A species Williams (= sieboldi) September of 2nd Torymus nobilis GB (Q. N/A (2010); Askew year robur) et al. (2013) Torymus scutellaris N/A Adults emerge Ormyrus nitidulus GB (Q. N/A February to April robur) rd of 3 Spring Caenacis lauta GB 2 Eupelmus azureus IT N/A 7.1 Eupelmus N/A spongipartus Eupelmus urozonus GB 2 3.6 Eupelmus vesicularis N/A Artholytus ocellus N/A Aprostocetus N/A cerricola Total ER = 21.4 Inquilines: Ceroptres clavicornis GB 2 Synergus apicalis N/A Synergus facialis N/A Synergus incrassatus GB (Q. 16 - 50 robur) Synergus N/A subterraneus Q. cerris Galls develop in Rare (eastern (Perilampus sp. nr No data No data Redfern et al. Q. petraea the summer on England) tristis) available available (2002); Stone Eurytoma adleriae et al., (2002);

Parasitism levels in oak galls 53

Aphelonyx cerricola Q. x hispanica shoots; mature in Eurytoma GB (Q. for this for this 1.4 Williams (Giraud)31 Q. ilex July brunniventris cerris)/IT species species (2010); Askew Q. ithaburensis Eurytoma pistaciae IT 3.8 et al. (2013); Asexual generation Q. suber Adults emerge Eurytoma setigera Ellis (2018) August to Sycophila biguttata GB (Q. 1.0 December 1st cerris)/IT year and January Sycophila variegata IT 0,3 to March 2nd year Megastigmus GB/IT 1.7 dorsalis Megastigmus synophri Torymus affinis Torymus auratus GB (Q. 3.0 cerris)/IT Torymus erucarum Torymus flavipes Torymus geranii Orymrus nitidulus GB (Q. 0.3 cerris)/IT Ormyrus pomaceus GB/IT 0.3 Ormyrus spp. IT 2.0 Cecidostiba fungosa GB (Q. 3.0 cerris)/IT Cecidostiba GB semifascia Cyrtoptyx robustus Hobbya stenonota GB/IT 9.6 Mesopolobus fasciiventris Mesopolobus GB sericeus Eupelmus azureus IT 3.0 Eupelmus cerris Eupelmus kiefferi IT 0.3

31 Aphelonyx cerricola is an invasive species which came across with Q. cerris. It was first discovered in Maidenhead in 1997 and expansion of its range is slow. Only the asexual generation is known. Redfern et al. (2002) and Williams (2010) both suggest that it is only found on Q. cerris in England. Askew et al. (2013) report a percentage representation of inquilines of 37% for asexual generation galls.

Parasitism levels in oak galls 54

Eupelmus spongipartus Eupelmus urozonus GB (Q. 1.0 cerris)/IT Reikosiella rostrata Aulogymnus arsames Aulogymnus gallarum Aprostocetus aethiops

( spp.) Gelis aerator GB Totol ER = 31.1 Inquilines: Ceroptres cerri Saphonecrus connatus Synergus apicalis GB Synergus facialis GB (Q. cerris) Synergus flavipes Synergus incrassatus GB Synergus thaumacerus Synergus variabilis GB (Q. cerris)/IT pallida Q. petraea Galls found May Common Periclistus sp. GB None None Redfern et al. (Olivier)32 Gall Q. robur to July on observed observed (2002); BRC- vegetative buds; Widespread Eurytoma adleriae N/A N/A DBIF (2008);

32 Askew et al. (2013) report a percentage representation of inquilines of 18% for the sexual generation of B. pallida. In addition to the tabulated data, Niblett (1944) reports that 229 chalcids (Torymidae/Pteromalidae) and four inquilines emerged from just 20 galls, equating to an ER of 1145% and an IR of 20%, respectively; the same author reports further data from another site where 263 chalcids (Torymidae/Pteromalidae) emerged from 11 galls, equating to an ER of 2390%. Ferracini et al. (2017) report that galls of the sexual generation of B. pallida are attacked by T. sinensis in the field (see Table 3 for further details).

Parasitism levels in oak galls 55

Sexual generation Q. cerris mature end of Eurytoma GB (Q. 5.9 None 2.1 BPGS Q. faginea June brunniventris robur)/IT observed Checklist Q. frainetto Eurytoma pistaciae IT 8.5 (2009); Q. lusitanica Adults emerge Eurytoma setigera N/A N/A Williams Q. pubescens May to August (2010); Askew Q. pyrenaica Eurytoma spinipes N/A N/A et al. (2013); Nature Spot Sycophila biguttata GB (Q. None 0 – 20 2.5 (2019) robur); IT observed (6.25) (Q. pubescens) Sycophila variegata GB (Q. 5.9 None robur) observed Megastigmus GB (Q. 5.9 0 – 10 (2.9) 0.1 dorsalis robur)/IT Torymus affinis GB (Q. 118 None 22.0 robur/Q. observed petraea); IT (Q. robur/Q. pubescens) Torymus auratus GB (Q. None 1 – 81 3.7 robur)/IT observed (36.75) Torymus flavipes GB (Q. None 22.5 – 224 11.5 robur/Q. observed (98.1) petraea)/IT Torymus geranii GB (Q. None 0 – 106 0.5 robur/Q. observed (41.5) petraea)/IT (Torymus laetus) N/A N/A Torymus ?macrurus N/A N/A Torymus notatus N/A N/A (Torymus N/A N/A pygmaeus) Torymus sp. 11.8 Torymus spp (males) 15 – 239 (129.75) Ormyrus nitidulus GB None None observed observed

Parasitism levels in oak galls 56

Ormyrus pomaceus GB (Q. 5.9 None 0.3 robur)/IT observed Ormryus spp. 0.3 Ormocerus vernalis N/A N/A Caenacis lauta N/A N/A Cecidostiba fungosa GB/IT None 0 – 30 (7.5) 16.7 observed Cecidostiba ilicina N/A N/A Cecidostiba GB (Q. None 0 – 10 (2.5) 19.6 semifascia robur/Q. observed petraea)/IT Cecidostiba 17.6 - N/A fungosa/ C. 35.3 semifascia Hobbya stenonota GB/IT 11.8 – None 8.7 29.4 observed Mesopolobus GB (Q. 5.9 None 0.05 amaenus robur)/IT observed Mesopolobus dubius GB (Q. 5.9 None robur) observed Mesopolobus GB/ IT (Q. 0 – 1.8 fasciiventris petraea/Q. (0.45) pubescens) Mesopolobus N/A N/A mediterraneus Mesopolobus GB (Q. 5.9 0 – 3 (0.75) 0.7 sericeus robur)/IT Mesopolobus tibialis GB (Q. 5.9 0 – 5a 0.1 robur)/IT (1.25) Mesopolobus GB (Q. 5.9 None 0.4 xanthocerus robur)/IT observed (Anastatus sp. nr N/A N/A catalonicus) Eupelmus azureus IT 9.2 Eupelmus kiefferi IT 0.2 Eupelmus N/A N/A spongipartus

Parasitism levels in oak galls 57

Eupelmus urozomus GB (Q. 5.9 None 10.3 robur/ Q. observed petraea)/IT Eupelmus vesicularis N/A N/A Eupelmus spp. 0.1 Reikosiella rostrata N/A N/A Aulogymnus N/A N/A arsames Aulogymnus N/A N/A gallarum Aulogymnus GB (Q. >118 None 50.8 skianeuros robur/Q. observed petraea)/IT Aprostocetus None None aethiops observed observed Aprostocetus IT N/A N/A 0.3 biorrhizae Aprostocetus N/A N/A ?cerricola Baryscapus anasillus N/A N/A Baryscapus N/A N/A berhidanus Baryscapus GB (Q. 5.9 None diaphantus robur) observed Baryscapus pallidae GB None None observed observed Baryscapus spp. 17.6 Mean total Total ER ER = 327.8 = 186.2 Inquilines: Ceroptres N/A N/A clavicornus

Synergus facialis GB 11.8 - 5 – 475 IT (Q. 29.4 (163.8) robur/Q. pubescens)

Synergus incrassatus N/A N/A

Parasitism levels in oak galls 58

Synergus pallicornis N/A N/A Synergus pallipes None 0 -5 (1.9) observed Synergus radiatus N/A N/A

Synergus ruficornis N/A N/A Synergus N/A N/A thaumacerus Synergus GB None None umbraculus observed observed Mean total IR = 165.6 Q. petraea Galls found all Common Torymus nobilus GB (Q. 12.5 No data No data Redfern et al. (Olivier) Q. robur year round on robur) available available (2002); BRC- roots; mature Torymus roboris GB None for this for this DBIF (2008); Asexual generation Q. pubescens October of 2nd observed species species Williams (= aptera) Q. pyrenaica year Cecidostiba N/A (2010); Askew ?fungosa et al. (2013); Adults emerge Cecidostiba N/A NatureSpot September to geganius (2019) December of 2nd Mesopolobus N/A year and March amaenus of 3rd year (Ichneumonid sp.) N/A

No inquilines known Callirhytis bella Q. petraea Galls found in Extremely rare No parasitoids No No data No data No data BRC-DBIF (Dettmer)33 Q. robur late autumn and known parasitoids available available available (2008); early winter on or for this for this for this Williams Sexual generation buds; mature in Inquilines: inquilines species species species (2010); Askew October Synergus tibialis known to et al. (2013); be Ellis (2018 Adults emerge associated April to July of in the UK 2nd year

33 Only the sexual generation of C. bella is known.

Parasitism levels in oak galls 59

Callirhytis Q. cerris Galls found Locally Eurytoma GB (Q. 0.8 No data No data BRC-DBIF erythrocephala Q. robur September to common/ Rare brunniventris cerris & Q. available available (2008); (Giraud) October on fruit and scattered robur) for this for this Williams on tree but Megastigmus GB (Q. 0.8 species species (2010); Askew Sexual generation spends three to dorsalis cerris & Q. et al. (2013); eight years on robur) Ellis (2018) the ground; matures in No known inquilines October

Adults emerge April to July Callirhytis Q. cerris Galls found Locally common Eurytoma GB (Q. No data No data No data Williams erythrocephala September to brunniventris cerris) available available available (2010); Askew (Giraud) October on fruit Megastigmus GB (Q. for this for this for this et al. (2013); on tree but dorsalis cerris) species species species Ellis (2018) Asexual generation spends three to Cecidostiba fungosa GB (Q. (= erythrostoma) eight years on cerris) the ground; ?Mesopolobus mature in dubius October Mesopolobus GB (Q. sericeus cerris) Adults emerge ?Aulogymnus sp. March to July No known inquilines Callirhytis glandium BRC-DBIF (Giraud)34 (2008) Cynips agama Q. petraea Galls of lateral Eurytoma Ellis (2018) (Hartig)35 Q. robur buds of young brunniventris shoots Sexual generation Q. frainetto Q. pubescens Synonym = Dryophanta agama Q. petraea Rare Eurytoma setigera

34 Redfern et al. (2002) discusses confusion surrounding Callirhytis species suggesting that old records of C. glandium are actually C. erythrocephala. 35 Williams (2010) states that the sexual generation of C. agama is not known.

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Cynips agama Yellow- Q. robur Galls found June Sycophila biguttata No No data No data No data Redfern et al. (Hartig) Pea Gall to November on Scattered; Torymus auratus parasitoids available available available (2002); BRC- Q. frainetto leaves; mature in localised Torymus cyaneus or for this for this for this DBIF (2008); Asexual generation Q. infectoria September Torymus geranii inquilines species species species Williams Q. macranthera Ormyrus pomaceus known to (2010); Askew Q. pubescens Adults emerge Mesopolobus be et al. (2013); September to fasciiventris associated Ellis (2018) November Eupelmus in the UK spongipartus Eupelmus urozomus Eupelmus vesicularis

Inquilines: Synergus facialis Synergus pallicornis Synergus pallipes Synergus umbraculus Cynips disticha Q. pubescens Galls found April Rare Torymus flavipes No No data No data No data Redfern et al. Hartig36 to May on Mesopolobus parasitoids available available available (2002); BRC- vegetative fasciiventris or for this for this for this DBIF (2008); Sexual generation buds/leaf margin Mesopolobus inquilines species species species Williams (= indistincta) at the end of the fuscipes known to (2010); Askew midrib or a thick Mesopolobus be et al. (2013); lateral vein; mediterraneus associated Ellis (2018) mature in May Mesopolobus tibialis in the UK Aulogymnus Adults emerge in obscuripes May

Cynips disticha Two-cell Q. petraea Galls found July Rare Eurytoma adleriae N/A No data Redfern et al. Hartig37 gall Q. robur to September on Eurytoma GB (Q. 3.4 available 4.4 (2002); BRC- the leaves; Local brumniventris petraea)/IT for this DBIF (2008); Asexual generation Q. coccifera mature at the Eurytoma pistaciae IT N/A species 4.4 Williams Q. faginea end of August Eurytoma setigera N/A (2010); Askew

36 Cynips disticha sexual generation cannot be distinguished from C. divisa in the field. 37 Askew et al. (2013) report a percentage representation of inquilines of 21% for the asexual generation of C. disticha.

Parasitism levels in oak galls 61

Q. ilex Sycophila biguttata N/A et al. (2013); Q. lusitanica Adults emerge Megastigmus N/A Ellis (2018) Q. pubescens September to dorsalis Q. pyrenaica November Torymus auratus GB (Q. 3.4 Q. suber petraea) Torymus cyaneus N/A Torymus flavipes GB None observed Torymus geranii GB None observed Ormyrus nitidulus N/A Ormyrus pomaceus N/A Ormyrus spp. IT N/A 2.2 Caenacis lauta N/A Cecidostiba fungosa N/A Cyrtoptyx robustus N/A Mesopolobus N/A fasciiventris Mesopolobus GB 3.4 sericeus Mesopolobus tibialis N/A Eupelmus vescularis N/A Aulogymnus N/A arsames Aulogymnus N/A ?gallarum Aulogymnus sp. N/A Aprostocetus N/A aethiops Total ER= 11.1 Inquilines: Synergus apicalis N/A Synergus facialis N/A Synergus pallicornis GB (Q. 6.9 – 17.2 robur) Synergus pallipes GB (Q. 27.6 – robur) 86.2

Parasitism levels in oak galls 62

Synergus radiatus GB None observed Synergus N/A thaumacerus Cynips divisa Red-Wart Q. petraea Galls found April Common Ormocerus vernalis No No No data No data Redfern et al. Hartig38 Gall Q. robur to June at end of Mesopolobus parasitoids parasitoid available available (2002); BRC- main or side mediterraneus or or for this for this DBIF (2008); Sexual generation Q. bicolor veins on leaves Mesopolobus tibialis inquilines inquiline species species Williams (= verrucosa) Q. frainetto or in the buds or Eupelmus urozonus known to attack (2010); Askew Q. infectoria flowers; mature Eupelmus vesicularis be observed et al. (2013); subsp. veneris in May Aulogymnus associated for this Ellis (2018) Q. pubescens skianeuros in the UK species Q. pyrenaica Adults emerge in May Inquilines: Synergus pallipes

Cynips divisa Red-Pea Q. petraea Galls found from Common Eurytoma GB (Q. >1.9 0 – 50a 0.4 Askew et al. Hartig39 Gall Q. robur mid-summer to brunniventris robur)/IT (11.1) (2002); October on Widespread Eurytoma pistaciae IT N/A N/A 0.4 Redfern et al. Asexual generation Q. borealis var. underside of Eurytoma setigera N/A N/A (2002); BRC- maxima leaves; mature Sycophila biguttata GB (Q. 0.04 0 – 0.55 DBIF (2008); Q. canariensis September robur) (0.1) Williams Q. faginea onwards Torymus auratus GB (Q. 0.1 – 0.2 0 – 1 (0.2) (2010); Ellis Q. frainetto robur) (2018) Q. infectoria Adults emerge Torymus GB 0.6 – 1.6 None subsp. veneris August to auratus/cingulatus observed st Q. lusitanica December 1 Torymus cyaneus GB (Q. >0.8 0 – 0.27 3.6 Q. x hispanica year and robur)/IT (0.04) Q. macranthera occasionally Torymus flavipes GB (Q. None None Q. pubescens robur) observed observed

38 Cynips divisa sexual generation cannot be distinguished from C. disticha in the field. Niblett (1944) reports an infestation rate of 7.1% for Synergus spp. and an emergence rate of 21.4% for Pteromalidae parasitoids from the sexual generation galls of C. divisa across two locations. 39 Niblett (1944) reports an inquiline (Synergus spp.) infestation rate ranging from 0 – 50% and a parasitoid (Torymidae/Eurytomidae/Pteromalidae) emergence rate ranging from 0 - 40% from nine separate collections of C. divisa asexual generation galls in southern England. Askew et al. (2013) report a percentage representation of inquilines of 21% for asexual generation galls of C. divisa. Stone et al. (2000; references cited within) quote a 0 – 50% percentage survival of galls over seven years of sampling but the study failed to identify whether this was a top-down or bottom-up effect.

Parasitism levels in oak galls 63

Q. pyrenaica January to Torymus geranii GB (Q. None None February 2nd year robur) observed observed Torymus spp. 0 – 10.5 (males) (2.2) Ormyrus nitidulus N/A N/A Ormyrus pomaceus N/A N/A Caenacis lauta GB (Q. 0.04 None robur) observed Cecidostiba fungosa N/A N/A Cecidostiba None 0 – 0.23 semifationis observed (0.04) Cyrtoptyx robustus N/A N/A Hobbya stenonota N/A N/A Mesopolobus GB None None amaenus observed observed Mesopolobus dubius GB (Q. 0.04 None robur) observed Mesopolobus GB (Q. None 0 – 2.2 (0.2) fasciiventris robur) observed Mesopolobus GB (Q. None 0 – 35 (1.8) sericeus robur) observed Mesopolobus >1.2 None sericeus/fasciiventris observed Mesopolobus tibialis N/A N/A Eupelmus N/A N/A spongipartus Eupelmus urozonus GB (Q. 0.07 0 – 1.2 (0.2) robur) Eupelmus vesicularis N/A N/A Aprostocetus GB (Q. 0.07 – None aethiops robur) 0.18 observed (Pediobius N/A N/A bruchicida) Mean total Total ER ER = 21.6 = 4.4 Inquilines: Ceroptres clavicornis N/A N/A Synergus facialis GB None 0 – 13.3 observed (3.7)

Parasitism levels in oak galls 64

Synergus incrassatus N/A N/A Synergus pallicornis GB (Q. 0.07 – 0.2 0 – 0.27 robur) (0.05) Synergus pallipes GB (Q. >0.82 0 – 200 robur) (41.7) Synergus radiatus GB (Q. None None robur) observed observed Synergus N/A N/A umbraculus Mean total IR = 45.4 Green Q. petraea Galls found April Uncommon Mesopolobus GB (Q. 8.3 No data No data Redfern et al. Hartig velvet- Q. robur to May on the fuscipes robur) available available (2002); BRC- bud gall vegetative buds; Mesopolobus tibialis N/A for this for this DBIF (2008); Sexual generation Q. frainetto mature end of species species Williams (= substituta) Q. pubescens May Inquilines: (2010); Askew Synergus facialis GB (Q. 25 - 50 et al. (2013); Adults emerge robur) Ellis (2018) May to June Synergus pallicornis GB None observed Cynips longiventris Striped- Q. petraea Galls found July Eurytoma adleriae N/A No data No data Redfern et al. Hartig pea gall Q. robur to October on Eurytoma GB (Q. 5.6 – 17.9 available available (2002); BRC- the leaves; brunniventris robur) for this for this DBIF (2008); Asexual generation Q. frainetto mature end of Sycophila biguttata GB (Q. 0.4 species species Williams Q. x hispanica September robur) (2010); Askew Q. pubescens Sycophila flavicollis N/A et al. (2013); Q. pyrenaica Adults emerge Megastigmus N/A Ellis (2018) September to dorsalis December 1st Megastigmus N/A year and January stigmatizans nd to March 2 year Torymus auratus GB (Q. 0.8 - 2 robur) Torymus GB 6.7 – 20.2 auratus/cingulatus Torymus cyaneus GB (Q. >8.7 robur) Torymus ?erucarum N/A

Parasitism levels in oak galls 65

Torymus flavipes GB None observed Torymus geranii GB (Q. None robur) observed Ormyrus nitidulus N/A Ormyrus pomaceus N/A Cecidostiba fungosa N/A Mesopolobus N/A amaenus Mesopolobus GB (Q. None fasciiventris robur) observed Mesopolobus GB (Q. None sericeus robur) observed Mesopolobus N/A fasciiventris/sericeus Pteromalus sp. N/A Eupelmus urozonus GB (Q. 0.8 robur) Aprostocetus GB (Q. >9.1 aethiops robur) Baryscapus N/A ?pallidae

Inquilines: Synergus apicalis N/A Synergus facialis N/A Synergus pallicornis GB 0.8 Synergus pallipes >9.1 Synergus radiatus GB None observed Violet-Egg Q. petraea Galls found April Common Sycophila biguttata N/A No data No data Redfern et al. L. Gall Q. robur to May on Torymus flavipes N/A available available (2002); BRC- vegetative buds; Torymus geranii N/A for this for this DBIF (2008); Sexual generation Q. cerris mature end of Caenacis lauta N/A species species Williams (= taschenbergi) Q. frainetto May Mesopolobus N/A (2010); Askew Q. x hispanica amaenus et al. (2013); Q. infectoria Mesopolobus dubius N/A Ellis (2018)

Parasitism levels in oak galls 66

Q. lusitanica Adults emerge Mesopolobus GB (Q. 4.5 Q. pubescens April to June fuscipes robur) Q. pyrenaica Mesopolobus tibialis N/A

Inquilines: Ceroptres clavicornis N/A Synergus facialis GB (Q. 36.3 – robur) 113.6 Cynips quercusfolii Cherry Q. petraea Galls found July Common and Eurytoma adleriae N/A No data Redfern et al. L.40 Gall Q. robur to October on widespread Eurytoma GB (Q. >7.8 available 0.3 (2002); BRC- leaves; mature brunniventris robur)/IT for this DBIF (2008); Asexual generation Q. cerris end of August Eurytoma setigera N/A species Williams Q. frainetto Sycophila biguttata GB (Q. >5.2 1.3 (2010); Askew Q. infectoria Adults emerge robur)/IT et al. (2013); Q. lusitanica September to Sycophila variegata N/A Ellis (2018); Q. macranthera December 1st Megastigmus GB (Q. 0.3 Nature Spot Q. pubescens year and January dorsalis robur) (2019) nd Q. pyrenaica to March 2 year Megastigmus IT N/A 0.1 stigmatizans Torymus auratus GB (Q. >16.4 8.3 robur/Q. petraea)/IT Torymus cyaneus GB (Q. 0.8 – 1.6 4.5 robur)/IT Torymus erucarum N/A Torymus flavipes GB None observed Torymus geranii GB/IT None 0.7 observed Torymus macrurus N/A Ormyrus nitidulus N/A Ormyrus pomaceus N/A Caenacis lauta N/A Cecidostiba fungosa N/A

40 Askew et al. (2013) report a percentage representation of inquilines of 41% for asexual generation galls of C. quercusfolii. Ferracini et al. (2017) report that galls of the asexual generation are attacked by T. sinensis in the field (see Table 3 for further details).

Parasitism levels in oak galls 67

Mesopolobus N/A amaenus Mesopolobus GB (Q. None fasciiventris robur) observed Mesopolobus GB (Q. None 0.1 sericeus robur/Q. observed petraea)/IT Mesopolobus GB 1.6 – 3.1 fasciiventris/sericeus Mesopolobus N/A ?tibialis Eupelmus N/A spongipartus Eupelmus urozonus N/A 0.4 Eupelmus vesicularis N/A Aulogymnus N/A gallarum Aulogymnus N/A trilineatus Aprostocetus GB (Q. 0.3 aethiops robur) Baryscapus N/A ?pallidae Total ER = 16.0 Inquilines: Ceroptres clavicornis N/A Saphonecrus N/A connatus Saphonecrus haimi N/A Synergus apicalis N/A Synergus facialis GB (Q. None robur) observed Synergus pallicornis GB (Q. 0.8 – 1.6 robur) Synergus pallipes GB (Q. 1.0 – 2.6 robur/Q. petraea)

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Synergus radiatus GB (Q. None robur) observed Synergus ruficornis N/A Synergus N/A thaumacerus Synergus tibialis N/A Synergus N/A umbraculus Schenck’s Q. petraea Galls found April Common Eurytoma GB (Q. 2.9 – 5.8 No data No data Redfern et al. (Schenck) Gall Q. robur to June on leaves brunniventris robur) available available (2002); BRC- and sometimes Torymus auratus GB 1 for this for this DBIF (2008); Sexual generation Q. canariensis flowers and Torymus flavipes GB (Q. None species species Williams Q. cerris buds; mature end robur) observed (2010); Askew Q. coccifera of May Ormocerus latus GB (Q. 5.8 – 19.4 et al. (2013); Q. faginea robur) Ellis (2018); Q. frainetto Adults emerge Ormocerus vernalis GB (Q. 1.9 – 4.9 Nature Spot Q. ilex April to July robur) (2019) Q. infectoria Mesopolobus dubius IT N/A subsp. veneris Mesopolobus GB (Q. 1 Q. lusitanica fasciiventris robur) Q. pubescens Mesopolobus GB (Q. 5.8 – 19.4 Q. pyrenaica fuscipes robur) Q. trojana Mesopolobus N/A mediterraneus Mesopolobus tibialis GB (Q. 5.8 – 19.4 robur) Eupelmus urozonus N/A Eupelmus vesicularis N/A Aulogymnus GB (Q. 5.8 – 19.4 arsames robur) Aulogymnus N/A gallarum Aprostocetus GB (Q. 1 aethiops robur) Pediobius saulius N/A

Inquilines: Synergus apicalis N/A

Parasitism levels in oak galls 69

Synergus pallipes GB (Q. None robur) observed Synergus sp. GB 2.9 – 5.8 Neuroterus albipes Smooth Q. petraea Galls found July Quite common Eurytoma N/A No data Redfern et al. (Schenck) Spangle Q. robur to September brunniventris available (2002); BRC- Gall onwards on for this DBIF (2008); Asexual generation Q. borealis var. leaves; mature species Williams (= laeviusculus) maxima end of August Sycophila biguttata N/A (2010); Askew Q. cerris Torymus ?auratus GB/IT 1.5 8.3 et al. (2013); Q. dalechampii Adults emerge Torymus flavipes GB (Q. None Ellis (2018); Q. frainetto February to April robur) observed Nature Spot Q. x of 2nd second Ormyrus pomaceus N/A (2019) haynaldiana year Arthrolytus nanus N/A Q. infectoria Mesopolobus GB (Q. 1.5 subsp. veneris fasciiventris robur) Q. lusitanica Mesopolobus N/A Q. pubescens sericeus Q. pyrenaica Mesopolobus tibialis GB (Q. 3 – 7.5 robur) Mesopolobus IT N/A 41.7 xanthocerus Eupelmus urozonus IT N/A 16.7 Pediobius clita GB (Q. 9 - 30 robur) Pediobius lysis GB 1.5 Total ER = 66.7 Inquilines: Synergus apicalis N/A Synergus facialis N/A Synergus pallicornis N/A Synergus pallipes GB 6 – 14.9 Synergus radiatus GB None observed Q. petraea Galls found Common Ormocerus vernalis GB (Q. None No data No data Redfern et al. Q. robur March to May on robur) observed available available (2002); BRC- leaves (terminal Mesopolobus >18.1 for this for this DBIF (2008); or axillary buds fasciiventris species species Williams

Parasitism levels in oak galls 70

Neuroterus Q. borealis var. or leaf stalks); Mesopolobus GB (Q. None (2010); Askew anthracinus maxima mature in May fuscipes robur) observed et al. (2013); (Curtis)41 Q. cerris Mesopolobus N/A Ellis (2018) Q. faginea Adults emerge mediterraneus (= Andricus Q. frainetto March to June Mesopolobus tibialis GB (Q. 0.9 anthracina) Q. infectoria robur)/IT and subsp. Mesopolobus GB 0.9 Sexual generation veneris xanthocerus Q. ithaburensis Aulogymnus N/A Q. lusitanica arsames Q. pontica Q. pubescens Inquilines: Q. pyrenaica Ceroptres clavicornis IT N/A Synergus facialis IT N/A Synergus pallipes N/A Synergus tibialis N/A Neuroterus Oyster Q. petraea Galls found mid- Very common Eurytoma GB (Q. 1.3 – 4.3 0 – 0.5 (1.7) 2.5 Redfern et al. anthracinus Gall Q. robur summer to brunniventris robur)/IT (2002); (Curtis)42 October on leaf Sycophila biguttata N/A N/A Williams Q. cerris midrib or main Torymus cingulatus 0.65 – 1.3 (2010); Askew (= Andricus Q. coccifera vein; mature Torymus ?cyaneus N/A N/A et al. (2013); anthracina) Q. faginea September Torymus flavipes N/A N/A Ellis (2018) Q. frainetto Torymus geranii GB (Q. None None Asexual generation C. x haynaldiana Adults emerge robur) observed observed Q. ilex September to Torymus spp. None st Q. infectoria December in 1 (males) observed and subsp. year and March Ormyrus ?nitidulus N/A N/A nd veneris to April in 2 Ormyrus pomaceus N/A N/A Q. ithaburensis year Ormyrus spp. IT N/A N/A 0.2 Q. lusitanica Cecidostiba fungosa IT N/A N/A 0.2 Q. macanthera Mesopolobus IT N/A N/A 0.4 Q. pubescens amaenus

41 Niblett (1994) reports that no parasitoids or inquilines emerged from a total of 172 sexual generation galls of N. anthracinus 42 Niblett (1944) reports an infestation range of 0.7 – 29.4% for S. pallipes and a range of 0.3 – 40.7% in chalcid (Eurytomidae/Pteromlaidae) emergence rates from five separate collections of asexual generation galls of N. anthracinus in Surrey, England during the early 1940s. Ferracini et al. (2017) report that galls of the asexual generation of N. anthracinus are attacked by T. sinensis in the field (see Table 3 for further details).

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Q. pyrenaica Mesopolobus GB (Q. >3 0 – 1.58 Q. rubra fasciiventris robur/Q. (0.4) Q. suber petraea) Mesopolobus GB (Q. 0.2 None 5.7 sericeus robur)/IT observed Mesopolobus spp. 0.4 Eupelmus kieffieri IT N/A N/A 0.4 Eupelmus urozonus GB (Q. 0.2 None 0.4 robur)/IT observed Eupelmus vesicularis N/A N/A Aulogymnus GB (Q. None None arsames robur) observed observed Aulogymnus N/A N/A gallarum (Cirrospilus diallus) GB (Q. None None robur) observed observed Aprostocetus GB (Q. 0.2 None aethiops (Q. robur) robur) observed Aprostocetus N/A N/A cerricola Baryscapus N/A N/A ?pallidae Baryscapus spp. IT N/A N/A 0.7 Mean total Total ER ER = 2.1 = 11.0 Inquilines: Ceroptres clavicornis N/A N/A Saphonecrus N/A N/A connatus Synergus facialis GB None 0 – 0.9 (0.2) observed Synergus pallicornis N/A N/A Synergus pallipes GB (Q. >4.3 0 – 50 (8.3) robur) Synergus radiatus GB (Q. None None robur) observed observed Synergus ruficornis N/A N/A Synergus N/A N/A thaumacerus

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Synergus N/A N/A umbraculus Mean total IR = 8.5 Neuroterus Blister- Q. petraea Galls found May Common Eurytoma GB (Q. 13 - 39 None No data Redfern et al. numismalis Gall Q. robur to October on brunniventris robur) observed available (2002); BRC- (Geoffroy in leaves; mature Eurytoma setigera N/A N/A for this DBIF (2008); Fourcroy) Q. cerris end of May Torymus auratus 1.3 species Williams Q. faginea Torymus flavipes GB (Q. None 0 – 237.5 (2010); Askew Sexual generation Q. infectoria Adults emerge robur) observed (118.8) et al. (2013); (= vesicator) and subsp. April to July Torymus spp. None None Ellis (2018) veneris (males) observed observed Q. pubescens Ormyrus pomaceus N/A N/A Q. pyrenaica Mesopolobus GB (Q. 2.3 – 6.5 None fasciiventris robur) observed Mesopolobus GB (Q. 1.3 None fuscipes robur) observed Mesopolobus N/A N/A mediterraneus Mesopolobus GB (Q. None 0 – 1.2 (0.6) sericeus petraea) observed Mesopolobus tibialis GB (Q. 10.4 – 3.6 – 15 robur) 32.5 (9.3) Eupelmus urozomus N/A N/A Aulogymnus GB (Q. 7.8 - 26 None arsames robur) observed Aulogymnus N/A N/A gallarum Aulogymnus N/A N/A skianeuros Cirrospilus diallus GB (Q. None None robur) observed observed (Cirrospilus viticola) N/A N/A Aprostocetus GB (Q. 1.3 None aethiops robur) observed Aprostocetus N/A N/A cerricola Minotetrastichus N/A N/A frontalis

Parasitism levels in oak galls 73

?Pediobius lysis N/A N/A Pediobius saulius N/A N/A (Closterocerus N/A N/A trifasciatus) Mean total ER = 128.7) Inquilines: Synergus facialis N/A N/A Synergus pallicornis N/A N/A Synergus pallipes GB (Q. >33.8 0 - 3.75 robur) (1.9) Mean total IR = 1.9 Neuroterus Silk- Q. petraea Galls found Very common Eurytoma N/A N/A No data Redfern et al. numismalis Button Q. robur August to and widespread brunniventris available (2002); BRC- (Geoffroy in Gall October on Sycophila biguttata N/A N/A for this DBIF (2008); Fourcroy)43 Q. borealis var. leaves; mature Torymus auratus GB 0.6 0 – 5.9 (1.0) species Williams maxima end of Torymus flavipes GB (Q. None None (2010); Askew Asexual generation Q. cerris September robur) observed observed et al. (2013); Q. dalechampii Torymus spp. GB None None Ellis (2018); Q. frainetto Adults emerge (males) observed observed NatureSpot Q. x hispanica February to April Ormyrus pomaceus N/A N/A (2019) nd Q. infectoria in 2 year Cecidostiba fungosa N/A N/A and subsp. Mesopolobus GB (Q. 0.3 None veneris fasciiventris robur) observed Q. lusitanica Mesopolobus tibialis GB (Q. 0.9 – 1.9 None Q. macranthera robur) observed Q. pubescens Aulogymnus GB None None Q. pyrenaica gallarum observed observed Q. rubra Pediobius lysis GB (Q. 6.3 0 – 58.8a Q. suber robur) (8.5)

Mean total ER = 9.6 Inquilines: Ceroptres clavicornis N/A N/A Synergus pallicornis N/A N/A

43 Askew et al. (2013) reports a percentage representation of inquilines of 1% for the asexual generation of N. numismalis.

Parasitism levels in oak galls 74

Synergus pallipes GB 1.3 – 3.1 None observed Synergus radiatus GB None None observed observed Neuroterus politus April-Bud Q. petraea Galls found April Common Mesopolobus GB (Q. 1.4 – 3.6 No data No data Redfern et al. Hartig Gall Q. robur to May on fuscipes robur) available available (2002); BRC- (= Neuroterus vegetative buds Mesopolobus tibialis GB for this for this DBIF (2008); aprilinus (Giraud)) Q. frainetto or leaf stalks; Mesopolobus GB species species Williams Q. pubescens mature in May xanthocerus (2010); Askew Sexual generation et al. (2013); Adults emerge Inquilines: NBN atlas April to May Ceroptres clavicornis (2019) Synergus umbraculus Neuroterus politus Q. petraea Galls found May Common Mesopolobus No No No data No data Redfern et al. Hartig Q. robur to June on the xanthocerus parasitoids parasitoid available available (2002); BRC- (= Neuroterus leaves or flowers; Aprostocetus or or for this for this DBIF (2008); aprilinus (Giraud)) Q. pubescens mature in May aethiops inquilines inquiline species species Williams known to attack (2010); Askew Asexual generation Adults emerge No known inquilines be observed et al. (2013) (= schlechtendali) July to August associated for this in the UK species Neuroterus Currant Q. petraea Galls found May Very common Eurytoma GB (Q. >6.0 None 1.0 Redfern et al. quercusbaccarum Gall Q. robur to June on and widespread brunniventris robur)/IT observed (2002); BRC- (L.)44 flowers, leaves Eurytoma setigera N/A N/A DBIF (2008); Q. bicolor and stems; Sycophila biguttata IT N/A N/A 0.3 Williams Sexual generation Q. canariensis mature May to Sycophila variegata N/A N/A (2010); Askew Q. cerris June Magastigmus N/A N/A et al. (2013); Q. dalechampii dorsalis Ellis (2018); Q. dentata Adults emerge Torymus affinis IT N/A N/A 0.3 Nature Spot Q. faginea May to July Torymus auratus GB (Q. >7.3 None (2019) Q. frainetto robur)/IT observed Q. infectoria & Torymus flavipes GB (Q. None 0 – 18 10.0 subsp. veneris robur)/IT observed (10.3) Q. lusitanica Torymus geranii N/A N/A

44 Askew et al. (2013) reports a percentage representation of inquilines of 27% for the sexual generation of N. quercusbaccarum.

Parasitism levels in oak galls 75

Q. macranthera Torymus N/A N/A Q. pontica ?longicalcar Q. pubescens Torymus notatus N/A N/A Q. pyrenaica Torymus spp. 0 – 30 (males) (11.9) Torymus spp. 1.0 Ormyrus pomaceus N/A N/A (Kaleva corynocera) N/A N/A Mesopolobus N/A N/A albitarsus Mesopolobus N/A N/A amaenus Mesopolobus dubius GB (Q. None None petraea) observed observed Mesopolobus IT N/A N/A fasciiventris Mesopolobus GB (Q. None None fuscipes petraea) observed observed Mesopolobus N/A N/A mediterraneus Mesopolobus GB (Q. 0.26 0 – 3.5 (1.4) 2.9 sericeus robur)/IT Mesopolobus tibialis GB (Q. 5.5 0 – 1.5 (0.6) 0.6 robur)/IT Mesopolobus GB (Q. None None xanthocerus petraea) observed observed Eupelmus N/A N/A spongipartus Eupelmus urozonus GB (Q. 0.26 None robur) observed Eupelmus vesicularis N/A N/A Aulogymnus GB (Q. >5.2 None arsames robur) observed Aulogymnus N/A N/A ?euedoreschus Aulogymnus GB None None gallarum observed observed Aulogymnus IT N/A N/A 0.6 skianeuros

Parasitism levels in oak galls 76

Aulogymnus N/A N/A testaceoviridis Aprostocetus N/A N/A aethiops ?Aprostocetus N/A N/A rufescens Baryscapus N/A N/A ?pallidae Pediobius N/A N/A ?rotundatus Mean total Total ER ER = 24.2 = 16.9 Inquilines:

Ceroptres cerri N/A N/A Saphonecrus N/A N/A connatus Synergus apicalis GB None None observed observed Synergus facialis GB/IT None 0 – 6.25 observed (1.4) Synergus pallicornis N/A N/A Synergus pallipes GB (Q. None 0 – 16 (7.3) robur)/IT observed Synergus GB/IT >6.0 None facialis/pallipes observed Synergus radiatus GB/IT None None observed observed Synergus ruficornis N/A N/A Synergus GB/IT None None thaumacerus observed observed Mean total IR = 8.7 Common Q. petraea and Galls found July Very common Eurytoma GB (Q. 1.2 None Redfern et al. Spangle subsp. to October on and widespread brunniventris robur) observed (2002); BRC- Gall pinnatiloba leaves; mature in Sycophila biguttata IT N/A N/A 0.5 DBIF (2008); Q. robur and August Sycophila variegata N/A N/A Williams subsp. Megastigmus N/A N/A (2010); Askew pedunculiflora dorsalis et al. (2013);

Parasitism levels in oak galls 77

Neuroterus Adults emerge Torymus affinis IT N/A N/A 0.3 Ellis (2018); quercusbaccarum Q. borealis January to May Torymus ?auratus 2.5 – 6.2 0 – 0.16 NatureSpot (L.)45 Q. canariensis of 2nd year (0.02) (2019) Q. cerris Torymus flavipes GB (Q. None None 11.7 Asexual generation Q. coccinea petraea/ observed observed (= lenticularis) Q. congesta Q. Q. dalechampii robur)/IT Q. faginea Torymus spp. GB None Q. frainetto (males) observed Q. x Ormyrus pomaceus N/A N/A haynaldiana Arthrolytus nanus N/A N/A Q. infectoria Mesopolobus N/A N/A and subsp. amaenus veneris Mesopolobus dubius GB (Q. 1.2 None Q. lusitanica robur) observed Q. macranthera Mesopolobus GB (Q. 1.2 None Q. palustris fasciiventris robur) observed Q. pubescens Mesopolobus IT N/A N/A 1.2 Q. pyrenaica sericeus Q. trojana Mesopolobus tibialis GB (Q. 2.5 – 6.2 None 1.9

(Q. robur) robur)/IT observed Eupelmus urozonus IT N/A N/A 0.2 Aulogymnus GB None 0 – 0.7 (0.1) arsames observed Aulogymnus GB (Q. 7.4 – 24.5 None 0.3 gallarum robur)/IT observed Aulogymnus GB None None gallarum f. pulchra observed observed Aulogymnus GB None 0 – 1.2 (0.2) skianeuros observed (Minotetrastichus N/A N/A frontalis) Pediobius clita None None observed observed

45 Askew et al. (2013) reports a percentage representation of inquilines of 27% for the asexual generation of N. quercusbaccarum. Ferracini et al. (2017) report that galls of the asexual generation are attacked by T. sinensis in the field (see Table 3 for further details).

Parasitism levels in oak galls 78

Pediobius lysis GB None 0 – 0.12 observed (0.05) Mean total Total ER ER = 0.3 = 16.2 Inquilines: Saphonecrus haimi N/A N/A Synergus facialis None 0 – 0.075 observed (0.01) Synergus pallicornis None None observed observed Synergus pallipes GB 9.9 - 31 0 – 1 (0.14) Synergus radiatus None None observed observed Synergus N/A N/A thaumacerus Mean total IR = 0.15) Neuroterus saliens Q. cerris Galls found on Rare Eurytoma GB No data No data No data Stone et al., (Kollar)46 fruit; mature brunniventris available available available (2002); April to May Torymus scutellaris GB for this for this for this Williams Sexual generation Cecidostiba fungosa GB species species species (2010) Adults emerge Cecidostiba GB June to August semifascia

No known inquilines Neuroterus saliens Q. cerris Galls found on Rare No known No data No data No data Stone et al., (Kollar)47 leaf veins and parasitoids or available available available (2002); petioles; mature inquilines for this for this for this Williams Asexual generation in September species species species (2010)

Adults emerge in the Spring

46 Neuroterus saliens is an invasive species which came across with Q. cerris. It was found in Great Britain for the first time in 2006 in London. Ellis (2018) and NatureSpot (2019) suggest that N. saliens is a synonym for Pesudoneuroterus saliens but the National Biodiversity Network (NBN, 2019) does not indicate this to be the case. Askew et al. (2013) report a percentage representation of inquilines of 15% for sexual generation galls. 47 Neuroterus saliens is an invasive species which came across with Q. cerris. It was found in Great Britain for the first time in 2006 in London. Ellis (2018) and NatureSpot (2019) suggest that N. saliens is a synonym for Pesudoneuroterus saliens but the National Biodiversity Network (NBN, 2019) does not indicate this to be the case.

Parasitism levels in oak galls 79

Neuroterus tricolor Hairy-Pea Q. petraea Galls found May Uncommon Eurytoma GB (Q. 1.9 No data No data Redfern et al. (Hartig) Gall Q. robur to August on brunniventris robur) available available (2002); BRC- leaves, mature Sycophila biguttata N/A for this for this DBIF (2008); Sexual generation Q. faginea end of June Torymus auratus GB 15.1 - 47 species species Williams Q. frainetto Torymus flavipes GB (Q. None (2010); Askew Q. ilex Adults emerge in robur) observed et al. (2013); Q. lusitanica July Ormyrus pomaceus N/A Ellis (2018); Q. pubescens Mesopolobus dubius N/A NatureSpot Q. pyrenaica Mesopolobus N/A (2019) Q. suber fasciiventris Mesopolobus N/A sericeus Mesopolobus tibialis GB (Q. 13.2 – robur) 39.6 Eupelmus vesicularis N/A Aulogymnus N/A arsames

Inquilines: Synergus facialis GB None observed Synergus pallipes GB 15.1 - 47 Synergus radiatus N/A Synergus GB None thaumacerus observed Neuroterus tricolor Cupped Q. petraea Galls found July Uncommon Eurytoma setigera No No data No data Redfern et al. (Hartig) Spangle Q. robur to October on Sycophila biguttata parasitoid available available (2002); BRC- Gall leaves (often on Torymus flavipes GB or for this for this DBIF (2008); Asexual generation Q. faginea lammas leaves); Torymus ?notatus inquiline species species Williams (= fumipennis) Q. frainetto mature end of Ormyrus pomaceus attack (2010); Askew Q. lusitanica August Eupelmus urozonus observed et al. (2013); Q. pubescens Aulogymnus for this Ellis (2018); Q. pyrenaica Adults emerge arsames species NatureSpot October to Pediobius lysis GB (2019) st November in 1 year and March Inquilines: to July in 2nd year Synergus facialis Synergus pallipes

Parasitism levels in oak galls 80

Synergus radiatus GB Synergus thaumacerus Plagiotrochus Q. ilex Galls are found Invasive, found Eurytoma No No data No data No data Robbins australis (Mayr)48 on the leaf in Glamorgan, brunniventris parasitoids available available available (2007); Askew Q. coccifera Wales in 2006 Eurytoma setigera or for this for this for this et al. (2013); Sexual generation Q. rotundifolia Sycophila biguttata inquilines species species species Ellis (2018) Q. suber Sycophila binotata known to Sycophila variegata be Torymus favardi associated Torymus flavipes in the UK Torymus notatus Ormyrus pomaceus Cecidostiba atra Cecidostiba ilicina Cyrtoptyx robustus Mesopolobus lichtensteini Mesopolobus tibialis Eupelmus seculatus Eupelmus urozonus Eupelmus vesicularis Aulogymnus arsames Aulogymnus bicolor Pediobius rotundatus

Inquilines: Ceroptres cerri Synergus crassicornis Synergus plagiotrochi Q. ilex Galls found Eurytoma No Robbins under the bark of brunniventris parasitoids (2007); Askew

48 Plagiotrochus australis is an invasive species which was discovered in 2007 (found in Glamorgan, Wales).

Parasitism levels in oak galls 81

Plagiotrochus Q. coccifera branches that are Invasive, found or et al. (2013); australis (Mayr)49 five to seven in Glamorgan, Inquilines: inquilines Ellis (2018) years old Wales in 2006 Ceroptres cerri known to Asexual generation Synergus be crassicornis associated Synergus ilicinus in the UK Plagiotrochus Q. ilex Galls found Invasive, found Sycophila variegata No data No data No data Robbins coriaceus (Mayr)50 protruding at in Glamorgan, Torymus notatus available available available (2007); Askew Q. coccifera either side of the Wales in 2006 Ormyrus pomaceus for this for this for this et al. (2013); Asexual generation Q. x hispanica leaf Cecidostiba atra species species species Ellis (2018) Q. suber Mesopolobus lichtensteini Mesopolobus xanthocerus Pediobius erdoesi IT Pediobius rotundatus

Inquilines: Ceroptres cerri Saphonecrus barbotini Plagiotrochus Q. ilex Galls found on Invasive, found Eurytoma adleriae No data No data No data Hancy and quercusilicis twigs in Cornwall, Eurytoma available available available Hancy (2004); (Fabricius)51 Q. coccifera England in 2004 brunniventris for this for this for this Ellis (2018) Sycophila biguttata species species species Sexual generation Sycophila binotata Sycophila flavicollis Sycophila variegata Megastigmus dorsalis Torymus flavipes Torymus notatus

49 Plagiotrochus australis is an invasive species which was discovered in 2007 (found in Glamorgan, Wales). 50 Plagiotrochus coriaceus is an invasive species which was discovered in 2006 (found in Glamorgan, Wales). A sexual generation is not known. 51 Plagiotrochus quercusilicis is an invasive species which was discovered in 2004 (found in Cornwall, England). One generation on Q. ilex, a second generation is suspected to exist.

Parasitism levels in oak galls 82

Ormyrus pomaceus Cecidostiba atra Cecidostiba ilicina Mesopolobus dubius Mesopolobus lichtensteini Mesopolobus IT mediterraneus Mesopolobus tarsatus Mesopolobus tibialis IT Mesopolobus xanthocerus Eupelmus seculatus Eupelmus spongipartus Eupelmus urozonus Eupelmus vesicularis Aulogymnus arsames Aulogymnus bicolor Aprostocetus aethiops Aprostocetua fusificola Pediobius rotundatus

Inquilines: Ceroptres cerri Synergus crassicornis Synergus plagiotrochi Pink-Bud Q. petraea Galls found April Locally common Torymus fastuosus GB (Q. 12.5 No data No data Redfern et al. Gall or Q. robur to June on shoot in the north and robur/Q. available available (2002); BRC- Pink-Wax and vegetative west petraea) for this for this DBIF (2008); Gall Q. frainetto Torymus formosus N/A species species Williams

Parasitism levels in oak galls 83

Trigonaspis Q. pubescens buds (trunks); Torymus nobilis N/A (2010); Askew megaptera Q. pyrenaica mature in May Mesopolobus dubius GB None et al. (2013); (Panzer)52 observed Ellis (2018) Adults emerge Mesopolobus GB (Q. None Sexual generation May to July fuscipes petraea) observed Mesopolobus tibialis GB (Q. None robur/Q. observed petraea) Aulogymnus GB (Q. None trilineatus robur/Q. observed petraea)

Inquilines: Synergus facialis GB None observed Synergus pallipes N/A Synergus GB 25 – 62.5 thaumacerus Trigonaspis Kidney Q. petraea Galls found Uncommon, Sycophila biguttata No data No data No data Redfern et al. megaptera (Panzer) Gall Q. robur September to mostly in the Torymus auratus available available available (2002); BRC- November on north and west Torymus ?cyaneus for this for this for this DBIF (2008); Asexual generation Q. cerris leaves; mature Torymus flavipes species species species Williams (= renum) Q. frainetto October Cecidostiba fungosa (2010); Askew Q. pubescens Mesopolobus GB (Q. et al. (2013); Q. pyrenaica Adults emerge fasciiventris robur) Ellis (2018) November to Aulogymnus sp. st December in 1 ?Pediobius lysis year and May to June of 2nd year Inquilines:

Synergus facialis Synergus pallicornis Synergus pallipes GB Synergus radiatus GB Synergus ruficornis

52 Ellis (2002) reports parasitoid emergence rates of 15% and 1.9% for M. dubius and M. tibialis, respectively, and an inquiline infestation rate of 13.2% for S. facialis in the sexual generation galls of T. megaptera.

Parasitism levels in oak galls 84

Synergus GB thaumacerus Synergus tibialis Trigonaspis Q. petraea Larvae found Rare and Eurytoma No No data No data No data BRC-DBIF synaspis (Hartig)53 Q. robur June to July on scattered brunniventris parasitoids available available available (2008); Askew vegetative buds Torymus fastuosus or for this for this for this et al. (2013) Sexual generation Q. faginea Mesopolobus inquilines species species species Q. lusitanica No information fasciiventris known to Q. pubescens available for Mesopolobus tibialis be Q. pyrenaica adult emergence associated Inquilines: in the UK Synergus facialis Synergus pallipes Synergus thaumacerus Trigonaspis Q. petraea Galls found Not known? Eurytoma No data No data No data BRC-DBIF synaspis (Hartig)54 Q. robur March to June on brunniventris available available available (2008); Askew leaves Sycophila biguttata for this for this for this et al. (2013); Asexual generation Q. lusitanica Sycophila iracemae species species species Ellis (2018) Q. pubescens Adults emerge Megastigmus June to July dorsalis Torymus auratus Torymus fastuosus Torymus geranii Ormyrus nitidulus Ormyrus pomaceus IT Cecidostiba fungosa Cyrtoptyx robustus Mesopolobus fasciiventris Mesopolobus graminum

53 Trigonaspis synaspis sexual generation is not listed in Redfern et al. (2002) or Williams (2010) as present in Great Britain although it is listed on BRC-DBIF (2008) as present. 54 Trigonaspis synaspis asexual generation is not listed in Redfern et al. (2002) or Williams (2010) as present in Great Britain although it is listed on BRC-DBIF (2008) as present.

Parasitism levels in oak galls 85

Mesopolobus xanthocerus Eupelmus urozonus Aprostocetus aethiops

Inquilines: Ceroptres cerri Synergus pallicornis Synergus pallipes Synergus physocerus IT Synergus thaumacerus

Parasitism levels in oak galls 86

Chapter 3. Interactions between oak galls, their associated communities and Torymus sinensis

Introduction of an alien species can result in changes in the structure and composition of ecosystems in many different ways and can lead to both detrimental and beneficial effects on biodiversity (e.g. through competition and predation, or by providing a new resource for native species to exploit) (Ehrenfeld, 2010; Konopka et al., 2017; Ferracini et al., 2018).

Askew (1961) points out that very few parasitoid species are continuously in flight between early spring and late autumn and that therefore the time when a gall is present on a tree will be a major influencing factor in which species attack it. Other factors are also likely to contribute to host specificity such as spatiotemporal traits (e.g. oak taxon, location of the gall on the tree, season and duration of development) and resource traits (e.g. host size, number of hosts per gall) (Askew, 1961; Stone et al., 2002; Hayward and Stone, 2005; Bailey et al., 2009). Morphological traits whilst not thought to provide complete protection from attack, as evidenced by the fact that most parasitoids and inquilines are capable of successfully attacking a wide variety of structurally different galls, are thought to provide a degree of protection with some resultant reduction in mortality (Askew, 1961; Stone et al., 2002; Hayward and Stone, 2005; Bailey et al., 2009). Morphological traits include:

 Nectar production to aid recruitment of which can significantly reduce parasitoid and inquiline attack;  The toughness of the gall – only parasitoids with strong will be able to drill into a tough gall, and drilling may also take longer increasing the risk of predation for the attacking parasitoid;  The thickness of the gall;  Number of larval chambers per gall (larvae developing in chambers deep within the gall are protected by those developing at the outer edges of the gall);  Other aspects of gall morphology e.g. sticky or hairy coatings, changes in colour, air spaces between the outer gall tissues and larval chamber.

Askew (1961) suggest that these traits can be used to predict which parasitoids attack which galls, with host plant being the most important criterion to consider. Work by Bailey et al. (2009) demonstrated that similar parasitoid communities occurred on galls with similar structural traits thereby providing support to the Enemy Hypothesis which predicts that galls with similar morphology will exclude similar groups of parasitoids and will therefore have similar communities within them. The Bailey et al. (2009) publication also consistently demonstrated that the structure of a parasitoid community within an oak gall could be predicted by components of the host spatiotemporal niche, most importantly by host oak and gall location on the tree. Host resource size was not found to be an influencing factor in the parasitoid community structure however, the number of hosts per gall and locularity were correlated (Bailey et al., 2009). These authors concluded that the patterns observed resulted mainly from partial niche specialisation of highly generalist parasitoids with broad host ranges (more than 20 hosts) rather than strict separation of enemies with narrower host ranges.

It is also important to take into account parasitoid and inquiline life traits when considering possible likely outcomes of parasitoids and inquilines on the actual gall former. For instance, in the case of the knopper gall (asexual generation of A. quercuscalicis), the larvae of the gall inducer inhabit an inner cell which is surrounded by an air space and then a thick outer wall. Parasitoids of the inner cell result in the death of the gall-inducer while the parasitoids and inquilines present within the outer wall do not kill the gall-inducer and therefore it is only the parasitoids that are found in the inner chambers that will impact on the population dynamics of the gall wasp (Hails et al., 1990).

Parasitism levels in oak galls 87

Information on these traits may be useful in enabling predictions of which galls could potentially be attacked by T. sinensis and which native parasitoid species are likely to attack the Oriental chestnut gall wasp. Studies and field observations in areas of Europe where T. sinensis has been released are now providing some information on these aspects; these studies have indicated that T. sinensis is not host-specific to sweet chestnut gall wasp and will adopt new hosts.

3.1 Evidence of parasitism by Torymus sinensis in oak galls

Prior to the release of T. sinensis in Italy in 2005, the only data available on host specificity of this parasitoid was from laboratory trials using the first consignment of the parasitoid, shipped to Italy during the previous year. These trials indicated that T. sinensis females did not oviposit or show any behavioural patterns associated with oviposition, when provided with galls of Cynips quercusfolii (asexual generation), A. kollari (asexual generation) or Mikiola fagi (Hartig) (a dipteran gall causer on the host plant Fagus sylvatica chosen because it would be present in the field at the time when T. sinensis would be ovipositing) (Quacchia et al., 2008).

Subsequent publications (EFSA, 2010; Gibbs et al., 2011) discuss the risk associated with the possible shift of T. sinensis to other hosts (reviewed by Down and Audsley, 2016) and a list of oak gall wasp species considered at risk based on matches to D. kuriphilus phenology was compiled and includes:

 Andricus curvator (sexual generation)  Andricus inflator (sexual generation)  Biorhiza pallida (sexual generation)  Neuroterus quercusbaccarum (sexual generation)  Andricus cydoniae (sexual generation)  Andricus grossulariae (sexual generation)  Andricus lucidus (sexual generation)  Andricus multiplicatus (sexual generation)  Dryocosmus cerriphilus (sexual and asexual generations)

Of these nine species, six of them (A. curvator, A. inflator, A. grossulariae, A. lucidus, B. pallida and N. quercusbaccarum are found in Great Britain (Table 1; BRC-DBIF, 2008).

Quacchia et al. (2014) report some pricking, albeit brief, when T. sinensis was presented with sexual generation galls of A. cydoniae, B. pallida and D. cerriphilus but state that no eggs were laid; no egg laying or oviposition behaviour was recorded when T. sinensis was presented with sexual generation galls of A. crispator, A. curvator, A. grossulariae or A. multiplicatus and asexual generation galls of D. cerriphilus. This compares with “no choice” tests conducted by Ferracini et al. (2015) who also observed attempted oviposition but no egg laying by T. sinensis in sexual generation galls of B. pallida galls and no attempted oviposition/egg laying with A. grossulariae, but in contrast they did observe oviposition in the sexual generation galls of A. curvator (galls were dissected so no information on potential development through to adulthood is given). Ferracini et al. (2015) also report no oviposition interest in N. quercusbaccarum (sexual generation). Further conflicting results are provided by Ferracini et al. (2017) when oviposition was recorded in A. grossulariae sexual generation galls but not in sexual generation A. curvator galls in “no choice” laboratory tests. Both probing and oviposition were observed in sexual generation A. cydoniae galls in contrast to results reported by Quacchia et al. (2014). Oviposition was also observed in asexual generation galls of A. lucidus but not in sexual generation galls of A. inflator, A. lucidus, A. multiplicatus, B. pallida and N. quercusbaccarum or the asexual generation galls of rosae. Torymus sinensis larvae were found in the non-target galls on which oviposition occurred (Ferracini et al., 2017). It must be noted

Parasitism levels in oak galls 88 too that Ferracini et al. (2015) provides the first report of non-target gall parasitism by T. sinensis in the field in Europe; three T. sinensis individuals emerged from a total of 856 B. pallida sexual generation galls (equating to an emergence rate of 0.35%).

A recent field study in Italy (Ferracini et al., 2017) revealed that T. sinensis is capable of parasitising some species of native oak galls in the field, and also alerts investigators to the possibility of different outcomes between laboratory and field studies. Native galls were collected over a three-year period from four species of oak (Q. robur, Q. petraea, Q. pubescens and Q. cerris) and wild rose (Rosa spp.) across 86 sites in nine regions of Italy, in areas where T. sinensis was present. A total of 14,512 non- target galls (from 30 species belonging to the genera Andricus, Aphelonyx, Biorhiza, Cynips, Diplolepis, Neuroterus and Synophrus) were collected, and 8708 chalcid parasitoids/inquilines were recorded emerging from these galls. The Torymidae family accounted for approximately 30% of the parasitoids with M. dorsalis, T. affinis and T. flavipes being the most represented species. Megastigmus dorsalis, A. skianeuros and S. biguttata were the species found emerging most frequently. Analysis of the Ferracini et al. (2017) results reveals that there are nine species of oak gall wasps that are native to the UK that were found to be parasitized by T. sinensis in the field in Italy (Table 3); these species are A. curvator (sexual generation), A. inflator (sexual generation), A. kollari (asexual generation), A. lignicolus (asexual generation), A. lucidus (asexual generation), B. pallida (sexual generation), C. quercusfolii (asexual generation), N. anthracinus (asexual generation) and N. quercusbaccarum (asexual generation). The parasitoid species known to be associated with these oak gall wasps in Great Britain (Table 1) are re-listed in Table 3 to aid the reader; it can be seen that there are at least nine species of oak cynipid wasps, 39 species of parasitoids and 12 species of inquilines within these communities that could be affected if T. sinensis adopts these non-target galls following release/natural arrival into Great Britain. Parasitoids include Torymus spp., Mesopolobus spp., Aulogymnus spp., Sycophila spp., Megastigmus spp. Ormyrus spp. and Cecidostiba spp. amongst others; the inquiline species are from across all three genera known to attack gall wasps (Ceroptres, Saphonecrus and Synergus). Effects may not necessariliy be detrimental but will be determined by the role of each species within the community e.g. parasitoid of the gall inducer, parasitoid of inquiline species, hyperparasitoid, lethal or non-lethal inquiline, and also the temporal succession of attack by these species. In addition to the non-target galls known to be present in Great Britain, a further six species of non-target galls not known to be present in Great Britain were also found to be parasitized (Table 3; Ferracini et al. 2017) and include A. caputmedusae (asexual generation), A. coronatus (asexual generation), A. cydoniae (sexual generation), A. dentimitratus (asexual generation), A. quercustozae (asexual generation) and Synophrus politus (sexual generation). A further 29 species of galls showed no indication of parasitism by T. sinensis in the field (Ferracini et al., 2017) and include species found in Great Brtain such as A. aries (asexual generation), A. foecundatrix (asexual generation), A. gallaeurnaeformis (asexual generation), A. grossulariae (asexual and sexual generation), A. inflator (asexual generation), A. lucidus (sexual generation), A. sieboldi (asexual generation), A. solitarius (asexual generation), Aphelonyx cerricola (asexual generation), C. disticha (asexual generation), C. divisa (asexual generation), N. albipes (asexual generation) and N. quercusbaccarum (sexual generation).

A total of 116 T. sinensis emerged from 15 species of oak galls in the Ferracini et al., (2017) study. With the exception of the sexual generations of A. curvator and A. inflator, the levels of T. sinensis parasitism in the non-target galls ranged from 0.1 to 1.6% (Table 3). However, of particular concern are the observations for the sexual generation galls of A. curvator and A. inflator; levels of parasitism by T. sinensis were higher (3.5% and 5.7%, respectively) and T. sinensis represented a significant portion of the total parasitoid complex that emerged from these galls (21.7% and 49.2%, respectively;

Parasitism levels in oak galls 89

Ferracini et al., 2017). Emergence rates of T. sinensis from sexual generation galls of B. pallida collected from the field during this study were comparable to those given by Ferracini et al. (2015) (0.5% and 0.35%, respectively).

The results of this field study highlight the potential danger in relying on laboratory studies to identify non-target effects with laboratory studies (Quacchia et al., 2014; Ferracini et al., 2015; Ferracini et al., 2017) failing to predict oviposition by, and successful emergence of, T. sinensis in some oak gall wasp species. Ferracini et al. (2017) conclude that data available from Italian field studies would indicate that T. sinensis does not exert any kind of population-level effect on non-target hosts as less than 5% mortality of non-target galls was observed. The study does not address any further potential direct/indirect non-target effects such as competition between T. sinensis and native oak gall wasp parasitoids. However, it is important to understand that the adoption of new hosts by a biological control agent is a dynamic process and could take many years (reported in Ferracini et al., 2017). Torymus sinensis is capable of inflicting density-dependent mortality on D. kuriphilus within a few years of introduction in its non-native ranges, as evidenced by its success in reducing pest populations of D. kuriphilus in Japan and Italy (Moriya et al., 1989; Quacchia et al., 2008; Ferracini and Alma, 2015); Stone et al. (2002) suggests that this is evidence for a “strong top-down effect in the dynamics of D. kuriphilus”, with “a normally generalist parasitoid acting as an effectively monophagous species on a superabundant host” raising the question “of whether the same parasitoid would act in a similarly density-dependent manner when in a community of multiple hosts”. How the adopted host-range evolves is also dependent on the success of the agent and population levels of the target pest, with success/and or low target pest levels likely to lead to a greater evolution of the non-target host range (Ferracini et al., 2017).

It is very difficult to investigate variation in oak gall wasp communities or compare different studies due to the rare or crytic nature of many of the gall wasp species or differences in sampling among host species and generations (Stone et al., 2002). Changes in the oak gall wasp community may also occur over time, and this natural variation will also need to be understood to ascertain whether T. sinensis is having effects on these communities. One two-year study in Finland (Kaartinen and Roslin, 2012) demonstrated that local oak gall food webs (individually analysed using samples from a 5km2 area) showed a high degree of consistency between years both in terms of species richness and quantitative structure but the actual species composition and linkage structure of the food webs changed quite considerably with time. Over the course of two years, 44% of the species that were present during the first year were not observed during the second year of the study, and 31% of the species observed in the second year were new. Data for the regional level (food webs were analysed as a group) indicated that the species composition was relatively stable with 77% of all species being present from one year to the next; 23% of the species present in the second year had not been recorded in the previous year, and 20% of the species recorded in the first year of the study were not recorded during the second year. Kaartinen and Roslin (2012) concluded that the rate at which species turned over was influenced by their ecological characteristics and that rare species, and species belonging to specific guilds, were more prone to local extinctions than the more abundant and generalist species.

Parasitism levels in oak galls 90

Table 3 Oak gall wasp species known to be attacked by the biocontrol agent Torymus sinensis in Italy. The table includes the percentage non-target gall parasitism (calculated as total number of parasitoids emerged/total number of galls collected), percentage non-target gall parasitism by T. sinensis and percentage relative dominance of T. sinensis within the parasitoid complex in each non-target gall species as calculated by Ferracini et al. (2017). The parasitoid species that are known to attack these non-target galls in Great Britain (if present) are also included to indicate the number and diversity of species associated with these communities in this country.

Oak gall wasp species Percent Percent parasitoid Percent relative Is the gall Percent Known UK parasitoids emergence of T. emergence (ER) dominance of T. present in parasitoid and inquilines sinensis from from each non- sinensis within Great Britain? emergence rate each non-target target gall species the parasitoid (ER) observed in gall species complex of each the UK as non-target gall reported by species Schönrogge & Crawley (2000) Andricus 1.6 43.9 3.6 No - caputmedusae (Asexual generation) Andricus coronatus 0.9 65.7 1.4 No - (Asexual generation) Andricus curvator 3.5 16.0 21.7 Yes 9.9 Eurytoma brunniventris (Sexual generation) Megastigmus dorsalis Torymus flavipes Torymus geranii Torymus notatus Mesopolobus albitarsus Mesopolobus amaenus Mesopolobus fasciiventris Mesopolobus fuscipes Mesopolobus sericeus Mesopolobus tibialis Eupelmus urozonus

Parasitism levels in oak galls 91

Aulogymnus arsames Aulogymnus gallarum

Synergus crassicornis Synergus facialis Synergus pallipes Synergus radiatus Synergus tibialis Andricus cydoniae 1.1 92.5 1.2 No - (Sexual generation) Andricus dentimitratus 1.6 198.4 0.8 No - (Asexual generation) Andricus inflator 5.7 11.6 49.2 Yes No data Megastigmus dorsalis (Sexual generation) available for this Torymus flavipes species55 Mesopolobus albitarsus? Aulogymnus arsames

Synergus crassicornis Andricus kollari 0.4 37.9 1.1 Yes 148.1 Eurytoma brunniventris (Asexual generation) Sycophila biguttata Sycophila variegata Megastigmus dorsalis Megastigmus stigmatizans Torymus auratus Torymus geranii Ormyrus nitidulus Caenacis lauta Cecidostiba fungosa

55 Although no data is available for A. curvator sexual generation galls in the Schönrogge & Crawley (2000) study, information is available from Askew (1961) and is presented in Table 1.

Parasitism levels in oak galls 92

Cecidostiba semifascia Hobbya stenonota Mesopolobus amaenus Mesopolobus dubius Mesopolobus fasciiventris Mesopolobus fuscipes Mesopolobus sericeus Mesopolobus tibialis Mesopolobus xanthocerus Eupelmus annulatus Eupelmus spongipartus Eupelmus urozonus Aulogymnus trilineatus

Ceroptres clavicornis Saphonecrus connatus Synergus crassicornis Synergus facialis Synergus pallicornis Synergus pallidipennis Synergus pallipes Synergus reinhardi Synergus umbraculus Andricus lignicolus 0.1 12.8 0.7 Yes 0.0 Eurytoma brunniventris (Asexual generation) Sycophila biguttata Megastigmus dorsalis Megastigmus stigmatizans Torymus auratus Torymus geranii

Parasitism levels in oak galls 93

Ormyrus nitidulus Mesopolobus amaenus Mesopolobus fasciiventris Mesopolobus fuscipes Mesopolobus sericeus Mesopolobus xanthocerus Eupelmus urozonus Aulogymnus skianeuros

Ceroptres clavicornis Saphonecrus connatus Synergus apicalis Synergus crassicornis Synergus facialis Synergus pallidipennis Synergus pallipes Synergus reinhardi Synergus umbraculus Andricus lucidus 0.3 189.4 0.2 Yes No data Eurytoma brunniventris (Asexual generation) available for this Sycophila biguttata species Torymus auratus Cecidostiba fungosa Mesopolobus sericeus Mesopolobus xanthocerus? Eupelmus urozonus

Ceroptres clavicornis Synergus umbraculus

Parasitism levels in oak galls 94

Andricus quercustozae 1.4 31.7 4.6 No - (Asexual generation) Biorhiza pallida 0.5 186.7 0.3 Yes 327.8 Periclistus sp. (Sexual generation) Eurytoma brunniventris Sycophila biguttata Sycophila variegata Megastigmus dorsalis Torymus affinis Torymus auratus Torymus flavipes Torymus geranii Ormyrus nitidulus Ormyrus pomaceus Cecidostiba fungosa Hobbya stenonota Mesopolobus amaenus Mesopolobus dubius Mesopolobus sericeus Mesopolobus tibialis Mesopolobus xanthocerus Eupelmus urozomus Aulogymnus skianeuros Aprostocetus aethiops Baryscapus diaphantus Baryscapus pallidae

Synergus facialis Synergus umbraculus Cynips quercusfolii 0.3 16.3 1.8 Yes No data Eurytoma brunniventris (Asexual generation) available for this Sycophila biguttata species Megastigmus dorsalis

Parasitism levels in oak galls 95

Torymus auratus Torymus cyaneus Torymus flavipes Torymus geranii Mesopolobus fasciiventris Mesopolobus sericeus Aprostocetus aethiops

Synergus facialis Synergus pallicornis Synergus pallipes Synergus radiatus Neuroterus 0.4 11.4 3.2 Yes 2.1 Eurytoma brunniventris anthracinus Torymus geranii (Asexual generation) Mesopolobus fasciiventris Mesopolobus sericeus Eupelmus urozonus Aulogymnus arsames Cirrospilus diallus Aprostocetus aethiops

Synergus facialis Synergus pallipes Synergus radiatus Neuroterus 0.2 16.4 1.1 Yes 0.3 Eurytoma brunniventris quercusbaccarum Torymus flavipes (Asexual generation) Mesopolobus dubius Mesopolobus fasciiventris Mesopolobus tibialis

Parasitism levels in oak galls 96

Aulogymnus gallarum Pediobius clita Pediobius lysis

Synergus pallicornis Synergus pallipes Synergus radiatus Synophrus politus 0.2 5.2 3.7 No - (Sexual generation)

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3.2 Parasitism of Oriental chestnut gall wasp galls by native oak gall wasp parasitoids

Native oak gall wasp parasitoids rapidly recruited to Oriental chestnut gall wasp in Italy, with four species recorded as emerging from D. kuriphilus galls collected in 2002 (the year Oriental chestnut gall wasp was discovered in Italy) and a further 11 species observed emerging from D. kuriphilus galls in 2003-2005 (Aebi et al., 2006). Gall attack rates, estimated per inhabitant, were low during these early years (0.5 – 1.6%; Aebi et al., 2006). Similar observations have been made in regions of Slovenia: in two areas where Oriental chestnut gall wasp was first observed during 2012/2013, galls were collected in 2013 and revealed six and nine native species of parasitoids inhabiting them, respectively (Kos et al., 2015). The recruitment of native parasitoids is discussed in detail in an earlier review by Down and Audsley (2016) on the biological control of Oriental chestnut gall wasp, and readers are encouraged to consult this review for detail. More information has been reported since 2016, and so an update is provided in the paragraphs below to complement the information available in the earlier review.

Numerous studies in Europe, mainly in Italy (Aebi et al., 2006; Panzavolta et al., 2013; Quacchia et al., 2013; Matošević and Melika, 2013; Alma et al., 2014; Francati et al., 2015; Kos et al., 2015; Colombari and Battisti, 2016; Fernandez-Conradi et al., 2018; Ferracini et al., 2018), have reported native oak gall wasp parasitoids attacking galls of the Oriental chestnut gall wasp. Alma et al. (2014) reported 38 native species known to be recruited to Oriental chestnut gall wasp in Italy, but that the association with D. kuriphilus has decreased over time. Rates of parasitism (percent emergence rates) are low 0 - 2.25% for the four most commonly found parasitoids (M. dorsalis, E. urozonus, E. annulatus, E. pistaciae) by Quacchia et al. (2013). Megastigmus dorsalis, T. flavipes, Mesopolobus spp. and Eupelmus spp. appear to be the most common species of native parasitoids to emerge from D. kuriphilus galls in Italy (Panzavolta et al., 2013; Alma et al., 2014; Francati et al., 2015; Bernardinelli et al., 2016). To date, a total of 40 species have been identified in Italy belonging to the Eupelmidae, Eurytomidae, Ormyridae, Pteromalidae and Torymidae) families, and are listed in Table 4. However, levels of parasitism in Oriental chestnut gall wasp galls by these native parasitoids remains low even though it might be expected to provide a level of control particularly in mixed stands of sweet chestnut and oak through associational resistance56. Rates of parasitism for Oriental chestnut gall wasp galls by native parasitoids in Italy are provided in Table 4 and overall emergence rates have been provided by a number of authors: 0.09 – 10.18% per average number of cells/gall (Francati et al., 2015); 0.51 – 5.74% per larval chamber (Panzavolta et al., 2013); 2.5 – 44.5% per gall (equating to 0.9 – 16.8% per larval chamber; Bernardinelli et al., 2016); 0.37 – 29.8% per gall (equating to 0.11 – 8.4% per larval chamber) during the years 2010-2012 during or shortly after release/arrival of T. sinensis and 0.0 – 7.14% per larvae in 2015; Colombari and Battisti (2016) and 0 – 35% per gall reported by Fernandez- Conradi et al. (2018).

Similar surveys have been conducted at four sites in Croatia (Matošević and Melika, 2013), chosen to represent differences in habitats (parkland with no oak trees present, coastal and inland chestnut forests containing oak (Q. petraea, Q. cerris, Q. pubescens) amongst other broadleaved species) and colonisation dates of D. kuriphilus. Galls, which were collected in 2011 and 2012, equating to two to five-years post introduction of D. kuriphilus depending on the site, were only collected in the spring i.e. were newly formed. The number of galls collected totalled 20,598 and from these 922 specimens

56 Associational resistance is a mechanism that explains why plants within a community that is species rich and heterospecific have a lower risk of invasion by herbivourous , and it has been suggested that this mechanism may also operate for invasive as well as native species (Guyot et al., 2015; Fernandez-Conradi et al., 2018) through the top-down biotic interactions that a species-rich community provides in terms of natural enemies.

Parasitism levels in oak galls 98 of parasitoids emerged. Across all sites, a total of 15 native species of chalcid parasitoids emerged and rates of emergence were low (Table 4). Torymus flavipes was the only species found at all sites in both years. Species of Eupelmus (E. annulatus and E. urozonus), M. dorsalis and M. tibialis were found relatively frequently whilst E. brunniventris, E. pistaciae, S. biguttata, O. pomaceus and T. auratus were all represented by less than five individuals in both years. As was found in Italy, initial recruitment of native parasitoids occurred very quickly (within two years), the diversity of native species found colonising D. kuriphilus galls increased with time reflecting the date of D. kuriphilus arrival and the composition of the site habitat, and then the recruitment process slowed down.

Oriental chestnut gall wasp was found in Slovenia for the first time in 2005. Ten years later (in 2015), T. sinensis was released as part of a classical biological control programme. Prior to release, both Oriential chestnut galls and native oak galls were sampled and details of the parasitoids that emerged from them recorded (Kos et al., 2015; see Table 4 for a list of the 27 species recorded emerging from D. kuriphilus galls). Both overwintering, and newly formed D. kuriphilus galls were collected between 2010 and 2013 in numerous regions across Slovenia. The most commonly found species emerging from galls of the Oriental chestnut gall wasp were T. flavipes, E. urozonus, E. annulatus and O. pomaceus accounting for 31%, 18%, 10% and 9.7% of all the emerging parasitoids, respectively (Kos et al., 2015). The overall mean emergence rate per gall (as a percentage) across seven sites was stated as 1.6% (ranging from 0.1 – 4.2%) for the overwintering galls and 8.4% (ranging from 1.0 – 38.8%) from the newly-formed galls (Kos et al., 2015). Kos et al. (2015) explain the higher emergence rates from the newly-formed galls as indicative of the fact that these emerging native parasitoids do not have synchronised life-cycles with D. kuriphilus.

A survey of Oriental chestnut galls in the Catalonia region of Spain in 2014 indicated that 14 species of native parasitoids, from five families of the Chalcidoidea, were associated with D. kuriphilus galls, including Mesopolobus lichtensteini (Mayr), which has not previously been reported as associated with D. kuriphilus (Jara-Chiquito et al., 2016). Seven native parasitoid species are reported to have recruited to D. kuriphilus galls in Hungary (Melika et al., 2013).

Matošević and Melika (2013) state that no inquiline species emerged from the galls collected in the Croatian survey; indeed, emergence of inquiline species has not been reported from other areas of Europe where surveys have been conducted, but whether this is because there was no inquiline emergence to report or because authors did not include these species in their studies is unclear. Inquilines are more sensitive to host divergence due to their phytophagous nature (Aebi et al., 2006) and this may explain why no inquilines have been reported as associated with galls of D. kuriphilus in its invasive range except for one report of a new inquiline species (Saphonecrus kuriphilusi) in Greece (Melika et al., 2017) and a single Synergus sp. reared from a D. kuriphilus gall in Japan (reported in Aebi et al., 2006). The lack of inquiline species in D. kuriphilus galls may also be a contributory factor in the low parasitoid emergence rates by native oak gall wasps observed from D. kuriphilus galls. As discussed earlier, some parasitoid species attack inquiline inhabitants of galls rather than the gall former itself, and the increase in parasitoid species/numbers associated with A. quercuscalicis (asexual generation) galls is thought to be correlated to inquiline attack of these galls.

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Table 4. Native oak gall wasp parasitoid species known to be associated with Dryocosmus kuriphilus in continental Europe (Italy, Croatia and Slovenia). Where available, rates of parasitism have been included. NB. Different authors have calculated rates of parasitism in different ways. Some have used the Standardised Emergence Rate (ER) = (number of parasitoids/number of galls) *100 i.e. percent emergence per gall; others have calculated percentages per larval chamber or per average number of chambers per gall, to account for the fact that D. kuriphilus is multilocular. Estimates that are divided by the average number of larval chambers per gall gives a more precise estimate of the level of parasitism (Kos et al., 2015). The table has been compiled using information from Aebi et al. (2006), Santi and Maini (2011) Panzavolta et al. (2013), Quacchia et al. (2013), Matošević and Melika (2013), Alma et al. (2014), Francati et al. (2015), Kos et al. (2015), Fernandez-Conradi et al. (2018) and Ferracini et al. (2018).

Family Species Associated with Rate of Associated with Rate of Associated with Parasitoid found D. kuriphilus in parasitism (%) D. kuriphilus in parasitism (%) D. kuriphilus in in Britain? Italy? (Italy) Croatia? (Croatia) Slovenia? Eurytomidae Eurytoma adleriae Yes Eurytoma brunniventris Yes 0 – 0.26 Yes 0 – 0.072 Yes Yes Eurytoma pistaciae Yes 0 – 1.76 Yes 0 – 0.036 Yes Eurytoma setigera Yes Sycophila biguttata Yes 0 – 0.08 Yes 0 – 0.036 Yes Yes Sycophila binotata Yes Sycophila flavicollis Yes Yes Sycophila iracemae Yes Sycophila variegata Yes 0 – 0.15 Yes 0 – 0.324 Yes Yes Ormyridae Ormyrus pomaceus Yes Yes 0 – 0.144 Yes Yes Ormyrus nitidulus Yes Yes Ormyrus sp. (pomaceus group) Yes Orymrus spp. Yes 0 – 0.2 Torymidae Megastigmus dorsalis Yes 0 - 1.98 Yes 0 – 4.929 Yes Yes Megastigmus almusiensis Yes Microdontomerus annulatus Yes Torymus auratus Yes 0 – 0.05 Yes 0 – 0.029 Yes Yes Torymus erucarum Yes Yes

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Torymus flavipes Yes 0 – 31.7557 Yes 0 – 3.814 Yes Yes Torymus formosus Yes Yes Torymus geranii Yes Yes 0 – 1.008 Yes Torymus scutellaris Yes Pteromalidae Cecidostiba semifascia Yes Yes Cecidostiba sp. Yes Mesopolobus amaenus Yes Yes 0 – 0.145 Yes Mesopolobus albitarsus Yes Yes Mesopolobus dubius Yes 0 – 0.648 Yes Mesopolobus fasciiventris Yes 0 – 0.03 Yes Yes Mesopolobus mediterraneus Yes Yes Yes Mesopolobus sericeus Yes 0 – 0.36 Yes 0 – 0.172 Yes Yes Mesopolobus tarsatus Yes 0 – 0.08 Yes Mesopolobus tibialis Yes 0 – 0.69 Yes 0 – 10.435 Yes Yes Mesopolobus spp. Yes Eupelmus Eupelmus annulatus Yes 0 – 1.23 Yes 0 – 0.209 Yes Yes Eupelmus azureus Yes Eupelmus confusus Yes Euplemus fulvipes Yes Eupelmus kiefferi Yes Eupelmus spongipartus Yes Yes Eupelmus splendens Yes Yes Eupelmus urozonus Yes 0 – 2.29 Yes 0 – 2.627 Yes Yes Eupelmus vesicularis Yes Eupelmus spp. Yes 0.7 Eulophidae Aulogymnus arsames Yes Yes Aulogymnus obscuripes Yes Aulogymnus skianeros Yes Yes Aulogymnus sp. Yes 0 – 0.05 Aprosocetus biorrhizae Yes Aprosocetus aethiops Yes Yes

57 Santi and Maini (2011) report an emergence rate of 31.75% for T. flavipes however, this is considerably higher than other reports. If this figure were to be excluded, the overall range from the remaining literature would be 0 – 3.17%.

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Aprosocetus glandicola Yes Aprosocetus sp. Yes 0 – 0.58 Baryscapus pallidae Yes Yes Baryscapus sp. Yes Yes Yes Minotetrastichus frontalis Pediobius chilaspidis Yes Pediobius saulius Yes Yes Pediobius sp. Yes

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3.3 Evidence for detrimental effects on native oak gall parasitoids in areas where Torymus sinensis has been released

In Japan, negative effects have been observed on the native parasitoid Torymus beneficus following release of the biocontrol agent T. sinensis. These detrimental effects are considered to be due to a mixture of displacement, hybridisation, inter-specific larval competition and reproductive ability (reviewed by Down and Audsley, 2016). In the US, a marginally significant negative correlation between parasitoids of oak gall wasps and T. sinensis has also been reported with this attributed to factors such as habitat, competition between adults for oviposition sites, larval competition and hyperparasitism (Cooper and Rieske, 2007).

To date, there is no direct evidence from Europe that T. sinensis has detrimental impacts on native oak gall parasitoids, but it is likely that insufficient time has passed since release for this to be properly ascertained. Whilst there is unequivocable evidence that T. sinensis is not host specific (it is capable of attacking at least 15 species of native oak galls in Italy), Ferracini et al. (2017) concluded from their field studies that T. sinensis does not currently exert any kind of population-level effect on non-target hosts as less than 5% mortality of non-target galls was observed. The authors do concede however, that the study does not address any further potential direct/indirect non-target effects such as competition between T. sinensis and native oak gall wasp parasitoids. Hybridisation between T. sinensis and native Torymus species has not been recorded in Italy thus far. Limited laboratory work has been conducted (using the native parasitoids T. affinis, T. auratus, T. flavipes, T. cyaneus and T. geranii) but no mating or mating behaviour was observed (Ferracini et al., 2017). A courtship dance was sometimes observed but the duration of the dance was always significanty less compared with the control pairings; no antennal contact, attempted mating or mating behaviour was ever recorded (Ferracini et al., 2017).

A predictive modelling study which modelled the composition and density of native parasitoid populations using predictive variables such as number of years since release of T. sinensis, occurrence of oak, type of chestnut formation (orchard or mixed forest) and latitude to attempt to establish whether T. sinensis in the agrosystem affects native oak gall wasp parasitoids (but specifically those known to be associated with Oriental chestnut gall wasp in the field) has been published (Ferracini et al., 2018). Prior to the modelling, a total of 102,000 chestnut galls were sampled from both chestnut orchards and mixed forests (containing oak, hophornbeam, wild cherry, and ash) and from these the emergence 4410 chalcid parasitoids in total were recorded, the most abundant of which were T. flavipes, species of Eupelmus and M. dorsalis. As expected, the model predicted impacts on the recruitment and accumulation of native parasitoids in chestnut gall wasps following the release of T. sinensis; the introduction of T. sinensis into the area had the greatest influence on the richness of native parasitoids; the model demonstrated that for every additional year present, T. sinensis contributed a 14% loss of native parasitoid species and a 32% reduction in the population density of the native parasitoids. With the exception of T. geranii, Eurytoma pistaciae and species of Euplemus, all native parasitoids, were negatively affected by the presence of T. sinensis; Ferracini et al. (2018) suggest that it is the ability of T. geranii, E. pistaciae and Euplemus spp. to act as facultative hyperpasitoids that protects them from negative effects in the presence of T. sinensis. This finding compares well with those of Colombari and Battisti (2016) who observed that there was a higher occurrence of native parasitoids in galls containing fewer larval chambers at sites where T. sinensis had not been released during their survey to investigate parasitism of D. kuriphilus galls. The occurrence of oak, particularly an increase in oak density within the area, also affected the native parasitoids, this time showing a positive affect on most of the parasitoid species (except for T. geranii,

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Eurytoma pistaciae and species of Euplemus). The combined effect of both presence of T. sinensis and oak density on recruitment and accumulation of native parasitoids, as predicted by the model, was a loss of 50% of the native oak parasitoid species five years after the release of T. sinensis (Ferracini et al., 2018).

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Summary

Fifty species of oak cynipid wasps have been identified as present in Great Britain, and many of them alternate between a sexual and an asexual generation, often completing their entire life-cycle within a year. The sexual and asexual generation galls are usually very different; they may be present on different parts of the tree and, as is the case for some Andricus species, may even require a different oak host species for female ovipostition and subsequent gall development. The galls induced by cynipid wasps in turn have a large array of chalcid parasitoids and cynipid inquiline species associated with them. Inquiline species may or may not induce the death of the gall former depending on the locations of their larval chambers within the gall, but they can provide an additional food source within the gall for some parasitoid species. Parasitoid species may attack the gall formers and/or the inquiline species and some species will even attack other species of parasitoid present within the gall. Hence, these galls represent complex but well-structured ecosystems with intricate food webs between all the inhabitants of the gall. Very few species of oak gall parasitoid and inquiline species are host specific. Some parasitoid species, such as Eurytoma brunniventris, Ormyrus pomaceus, Eupelmus urozonus and Sycophila biguttata are known to have 80 or more host species across the west Palaearctic region. However, the galls formed by the two generations of cynipid wasps are often attacked by a different set of parasitoid and inquiline species although galls of the same generation of closely related gall wasps may share similar parasitoid and inquiline species. As can be seen from the data presented in Table 1, levels of parasitism and inquiline attack rates (as determined by the numbers of emerging adults) can be highly variable; multilocular galls have the potential to produce a greater number of parasitoid adults than unilocular galls, and this number can be greater still if the gall is inhabitated by inquiline species too.

Any invasive parasitoid species has the potential to impact upon these complex host-parasitoid- inquiline relationships should it adopt a native gall wasp species as an alternative non-target host. As such, if a non-native parasitoid species is under consideration as a biocontrol agent for a non-native pest, then a risk assessment of its potential non-host range should be conducted. If released into the environment, monitoring for non-host parasitism would be advisable. Monitoring for any such impacts in the field following release requires knowledge of the species associated with native gall wasps and their levels of parasitism/attack; Table 1 provides such baseline data for Great Britain or at least as far as available information in the literature enabled.

Risk assessments for the release of Torymus sinensis to control the Oriental chestnut gall wasp identified nine gall wasp species, on paper, that were considered potential non-target hosts for T. sinensis. However, laboratory and field studies conducted in Italy to assess the potential non-target host range of T. sinensis have highlighted the dangers of relying solely on laboratory investigations to answer such questions, with laboratory experiments producing conflicting results. Fifteen species of oak gall wasp have been identified as non-target hosts for T. sinensis in field studies conducted in Italy following the release of the non-native parasitoid to control the Oriental chestnut gall wasp. Of these 15 species, the sexual generation galls of A. curvator and A. inflator suffered the most significant attack from T. sinensis; whilst the emergence rates of T. sinensis were low (3.5% and 5.7%, respectively), the relative dominance of T. sinensis within the parasitoid complex of these two galls species was high (21% and 49%, respectively). Adoption of new-hosts is a dynamic process and it remains to be seen how this will impact on these native gall wasps and their associated parasitoids.

To date, 48 species of native parasitoids have been observed to attack the Oriental chesnut gall wasp in its invasive range in Europe. However, levels of attack remain low with emergence rates for each individual species typically below 2%.

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