Synergus variabilis Mayr, 1872

Askew, Richard R., Melika, George, Pujade-Villar, Juli, Schönrogge, Karsten, Stone, Graham N. & Nieves-Aldrey, José Luis, 2013, Catalogue of parasitoids and inquilines in cynipid oak galls in the West Palaearctic, Zootaxa 3643 (1), pp. 1-133 : 119-122

Synergus variabilis Mayr, 1872

A. grossulariae sx Dryocosmus cerriphilus sx, ag

Aphelonyx cerricola ag Pseudoneuroterus macropterus ag

Cerroneuroterus lanuginosus ag Synophrus politus

Chilaspis nitida ag

Comments

A significant difference between the cynipid oak gall fauna (catalogued here) and that in galls of Cynipidae attacking mainly herbaceous and shrubby plants ( Askew et al. 2006) is the relative abundance of inquiline cynipids ( Synergus species and the small genera Ceroptres and Saphonecrus ) in oak galls. The larger numbers of inquilines ( Table 1 ) are usually associated with those galls having a thick layer of tissue surrounding the central gall wasp larval chamber providing space for several non-lethal inquiline chambers. Small thin-walled galls, in contrast, can accommodate only a solitary lethal inquiline. The presence of inquilines in a gall provides an additional resource for exploitation by parasitoids. A marked increase in the number of species of Chalcidoidea in asexual generation galls of Andricus quercuscalicis coincided with the colonization of the gall by Synergus ( Hails et al. 1990, Schönrogge et al. 1996).

About one hundred morphospecies of Chalcidoidea are parasitoids in oak galls of Cynipini in the West Palaearctic, distributed over six families: Eurytomidae (10 species), Torymidae (21 species), Ormyridae (2 species, but almost certainly additional species are present), Pteromalidae (29 species), Eupelmidae (8 species) and Eulophidae (29 species). Aylacini , Diplolepidini and Pediaspidini support similar parasitoid complements but with more species of Eurytomidae and fewer of Pteromalidae , and cynipid inquilines ( Periclistus ) are present only in Diplolepis galls on Rosa ( Askew et al. 2006) .

The genus Torymus is represented in oak galls by most species (16), followed by Mesopolobus (12) and Aulogymnus (9). Aulogymnus species are only exceptionally, and Mesopolobus species seldom, found in cynipid galls other than on oak. Torymus are common inhabitants in galls of all tribes, although a mostly different set of species is associated with each. Apart from some Eupelmidae , relatively few chalcid species have been associated with more than a single tribe of gall wasps ( Table 2). It is usually species normally found in galls of Cynipini which appear to invade galls of the other tribes, particularly those of Diplolepidini .

* Mesopolobus graminum is a common parasitoid of Tetramesa (Eurytomidae) in grass stems and is only abnormally associated with Cynipidae ( Rosen 1960) .

The long lists of host galls presented above under the chalcid parasitoids in Cynipini galls clearly show that a broad host gall range is usual. Eurytoma brunniventris has the highest number (100) of recorded host galls, followed by Ormyrus pomaceus (96), Eupelmus urozonus (87) and Sycophila biguttata (80), but Torymus flavipes , with only 40 host galls, was the most commonly reared parasitoid ( Table 3). The numbers of specimens of the more abundantly reared species bear very little relationship to the numbers of host galls. E. brunniventris can apparently feed as a larva on any other gall inhabitant and also on gall tissue ( Claridge & Askew 1960). Larvae of most other species do not consume plant tissue but in other respects are also broadly polyphagous. T. flavipes is more host gall restricted than E. brunniventris , but much less so than T. affinis . Over six thousand individuals of the latter were reared from only six gall types, 99 percent emerging from sexual generation galls of Biorhiza pallida . Of species recorded in large numbers, the most extreme host gall specialisation is seen in Cecidostiba geganius, 1119 individuals being obtained from asexual generation galls of Andricus quercusradicis but otherwise with only a single individual reared from an asexual generation gall of Biorhiza pallida and a published record of its presence in asexual generation galls of Andricus kollari . In summary, most species of chalcid parasitoid seem to have the potential to develop in a wide range of oak gall types, but in practice a large potential host gall range is more or less restricted.

Asexual generations on oaks of Section Quercus sensu stricto, sexual generations on Section Cerris oaks: Andricus grossulariae 76 Andricus lucidus 29 Andricus quercuscalicis 26 Andricus kollari 1

Both generations on oaks of Section Quercus sensu stricto Neuroterus quercusbaccarum 47 Neuroterus numismalis 11 Neuroterus albipes 5 Andricus quercusradicis 1

Both generations on oaks of Section Cerris Neuroterus saliens 21 Chilaspis nitida 15

The specific identity of the host tree limits the host gall range of a few species of parasitoid. Torymus cerri and Eupelmus cerris probably attack galls growing only on Quercus subgenus Quercus section Cerris (Q. cerris , Q. suber). A small group of species appears to be strongly, although rarely exclusively, associated with Plagiotrochus galls which grow on evergreen Quercus section Cerris (especially Q. coccifera and Q. ilex) in the Mediterranean region: Sycophila binotata , Cecidostiba atra and C. ilicina , Mesopolobus lichtensteini and possibly M. mediterraneus , and Pediobius rotundatus . Two other species, Eupelmus seculatus and Aprostocetus fusificola , are known only from Plagiotrochus galls but in small numbers.

Characteristics of the gall also affect the composition of its parasitoid fauna. The large, woody, asexual generation bud galls of Andricus species in the kollari -group have relatively similar parasitoid complements which are dominated by Eurytoma brunniventris , Megastigmus species and Ormyrus nitidulus , with Cecidostiba fungosa and Sycophila biguttata well-represented. Leaf undersurface galls of asexual generation Cynips species support large numbers of Torymus cyaneus , and galls of asexual generation Andricus quercusradicis , A. sieboldi , A. rhyzomae , A. quercuscorticis , Trigonaspis megaptera and Biorhiza pallida , all of which develop on the bark of trunk, lower branches or roots of section Quercus sensu stricto, house species of Torymus assigned to the erucarum -group ( T. erucarum , T. formosus , T. nobilis , T. roboris , T. scutellaris ). Thus, the position and gross morphology of a gall are important in determining the species of chalcid parasitoid which will be associated with it. In a restricted area in England it was shown that the parasitoid fauna in cynipid oak galls was strongly correlated with gall morphology, position on the tree and season of growth ( Askew 1961b). In the more broadly-based data presented in this catalogue, however, such determining factors tend to become blurred by misidentifications, the presence of cryptic species and geographical effects.

Because galls of alternate generations of the same gall wasp species are very different, they usually support very different parasitoid faunas ( Table 4). Andricus grossulariae appears to be exceptional, however, even though its sexual generation is in a catkin gall on Quercus cerris whilst the asexual generation is in an acorn gall on Q. robur. Overall percentage similarity (sum of the lesser percentage representations of all shared parasitoid species) between the sets of chalcid parasitoids associated with the two generations is a remarkably high 76%, a figure much higher than the intergeneration similarity recorded for any other gall wasp ( Table 4). No explanation of this apparent anomaly can be suggested.