Butlletí de la Institució Catalana d’Història Natural, 84: 31-34. 2020 ISSN 2013-3987 (online edition): ISSN: 1133-6889 (print edition)31 nota breu NOTA BREU

Re-instatement of the species name erythrosoma (Dettmer, 1933), with comments on other Callirhytis species (: Cynipidae) Restitució del nom de l’espècie Callirhytis erythrosoma (Dettmer, 1933), amb comentaris sobre altres espècies de Callirhytis (Hymenoptera: Cynipidae)

James A. Nicholls * & Juli Pujade-Villar **

* CSIRO, Australian National Collection. Clunies Ross Street. Acton, ACT 2601, Australia. A/e: [email protected] ** Department of Biology. Barcelona University. 08028 Barcelona, Catalonia. A/e: [email protected]

Corresponding author: Juli Pujade-Villar. A/e: [email protected]

Rebut: 05.03.2020. Acceptat: 14.03.2020. Publicat: 31.03.2020

Förster (1869) first described Callirhytis to include some diapause in these asexual galls for between one to eight years European gall forming cynipid species that uniquely present (Barbotin† pers. comm., after Nieves-Aldrey 1992). transversely striated sculpturing on the scutum and malar Both generations are known for C. glandium and C. rufes- sulcus. Since then some authors, without considering these cens following Barbotin’s experimental studies, published by diagnostic characters, have treated Callirhytis as a subgenus Nieves-Aldrey (1992). Callirhytis comantis is known only of : Andricus (Callirhytis) possessing simple tarsal from its sexual generation and C. reticulatus from its asexual claws, while the nominal subgenus Andricus (Andricus) hav- generation, and this pairing could represent alternate gen- ing tarsal claws with a basal lobe (e.g. Mayr 1881; Ashmead erations of the same biological species (Maisuradze 1961). 1885; Cameron 1893; Dalla Torre 1893; Kieffer 1897-1901). The taxonomic status of C. bella is uncertain. This species, Later, Mayr (1902) restored the generic status of Callirhytis known only from females of the suspected sexual generation, and Dalla Torre & Kieffer (1910) followed suit, as the tarsal emerges in April-May from cryptic galls located inside small claws are not a diagnostic character in Callirhytis (Nieves- buds on Q. robur and Q. petraea. It has rarely been collected, Aldrey 1992). Weld (1922, 1926, 1952) included many Ne- only being known from the Netherlands and British Islands arctic species in this genus, again ignoring the diagnostic (Nieves-Aldrey 1992) and France (new record; galls and characters given by Förster (1869), and as result of this Cal- adults collected from «Reserve Naturelle Forêt de la Mas- lirhytis has become a very chaotic genus (herein termed Cal- sane/Banyuls Sur Mer»). Morphologically it is very similar lirhytis «sensu lato»). Melika & Abrahamson (2002) pointed to the sexual generation of C. glandium, from which it can out that of the 115 Nearctic species of Callirhytis named in only be distinguished through having smaller and more sepa- Burks (1979), only 15 are Callirhytis «sensu stricto». Con- rated antennae as well as by slight differences in pronotal and sistent with this, in recent years two new genera (Zapatella mesopleural sculpturing (Nieves-Aldrey 1992). However, the Pujade-Villar & Melika, 2012 and Melikaiella Pujade-Villar, sexual generation of C. glandium emerges much later in late 2014) have been described to include some of these incor- July and August. This early emergence of C. bella is more rectly assigned Nearctic Callirhytis (Pujade-Villar et al. typical of asexual forms of European Callirhytis, although its 2012, 2014), and further revisionary work on Nearctic Calli- host plant association and morphology imply it is a sexual rhytis is ongoing. According to Pénzes et al. (2018), a single generation. Finally, C. hartigi Förster, 1869 was proposed Callirhytis species also occurs in the Eastern Palaearctic (C. as the possible sexual generation of C. erythrocephala by glanduliferae Monzen, 1953). Nieves-Aldrey (1992) and was formally synonymized with Callirhytis is represented in the Western Palaearctic re- C. erythrocephala by Pujade-Villar et al. (2005) after unpub- gion by six species (Pujade-Villar et al., 2005): four are lished studies by both Folliot (in 1964-1967) and Barbotin† present in western and central Europe (C. bella (Dettmer, (in 1971-1986) independently closed this species’ life-cycle. 1930); C. erythrocephala (Giraud, 1959); C. glandium (Gi- However, the asexual generation of C. erythrocephala as raud, 1959) and C. rufescens (Mayr, 1882)), and two species defined by Nieves-Aldrey (1992) presents some taxonomic are known from the Caucasus region (C. comantis Belizin & issues. Dettmer (1933) described two asexual species: Cal- Maisuradze, 1961 and C. reticulatus Belizin & Maisuradze, lirhytis erythrosoma and C. erythrostoma. Both were syno- 1961). The sexual generations of the European species induce nymized as being the asexual generation of C. erythrocepha- summer galls in twigs (rarely in buds) of belonging to la (Giraud, 1859) by Nieves-Aldrey (1992), although this Quercus section Quercus and the asexual generations induce was contrary to Barbotin’s unpublished experimental notes galls inside acorns of Quercus section Cerris oaks; larvae can stating that both species induce different asexual galls. Cal-

DOI: 10.2436/20.1502.01.35 Butlletí ICHN 84, 2020 32 J. A. NICHOLLS & J. PUJADE-VILLAR NOTA BREU lirhytis erythrocephala (= C. erythrostoma) produces a coa- C. erythrosoma Matrafured, Hungary lescent and hard almond-shaped gall within the endocarpium C. erythrosoma of an acorn resulting from the fusing of multiple unilocular Guyla, Hungary larval cells into one large agglomerate, while in contrast C. C. erythrosoma erythrosoma induces a hemispherical group of gall chambers Saint Malo, France which can usually be separated into individual larval cham- C. erythrosoma Saint Malo, France bers (Pujade-Villar et al., 2005). The asexual females of both forms are similar but according Barbotin’s† notes can be C. erythrosoma Copenhagen, Denmark easily distinguished: females reared from galls of C. eryth- C. erythrosoma rosoma are red-yellowish while those reared from the galls Copenhagen, Denmark of C. erythrocephala have a black mesosoma. One way to C. erythrosoma resolve the status of these species requires experimental rear- Copenhagen, Denmark ings that follow individuals through multiple generational C. erythrocephala cycles, which is a long and difficult process. Alternatively, a Saint Malo, France C. erythrocephala simpler method examining DNA sequence variation can be Saint Malo, France employed; recent work has demonstrated the efficacy of this C. rufescens method for discriminating among sister species in cynipids Algatocin, Spain and matching otherwise unpaired generations (e.g. Stone et C. rufescens al. 2008; Nicholls et al. 2012, 2018). Algatocin, Spain To this end, DNA was extracted from two adult individu- C. glandium als of each asexual European Callirhytis species previously Gyula, Hungary recognised in the literature as being morphologically dis- C. glandium Piedralaves, Spain tinct: C. erythrostoma, C. erythrosoma, C. glandium and C. 0.008 subs/site rufescens. The adults of C. erythrostoma and C. erythrosoma Melikaiella tumifica were reared from Q. cerris acorns collected at the same local- Figure 1. Neighbour-joining tree based upon cytochrome b gene se- ity, St Malo in north-western France, so provide a test of the quences obtained from the four Callirhytis species present in Europe genetic distinctiveness of these two morphotypes in sympa- and with known asexual generations. Terminals are labelled with their try. In addition, five larvae dissected fromQ. cerris acorns in species name and collection location. Hungary (two individuals) and Denmark (three individuals) were also extracted. A 433 base pair section of the mitochon- drial cytochrome b gene was sequenced for each individual, in general (Hebert et al., 2003). All the sequenced larvae ap- as this gene has been demonstrated to provide species-level peared to be from the species C. erythrosoma, and within resolution within cynipids (Nicholls et al. 2012; Tang et al. this species the divergence associated with geographically- 2016a, b; Cerasa et al. 2018; Nicholls et al. 2018; Tang et separated samples was low (on average 0.5%; range 0-0.9%), al. 2020). Variation within and between putative species was again consistent with there being two genetically discrete calculated, and a neighbour-joining tree was constructed us- species previously included in the C. erythrocephala com- ing HKY genetic distances and rooted using the Nearctic spe- plex. All new sequences are deposited in GenBank, acces- cies Melikaiella tumifica (GenBank accession MG821060). sions MT152275-MT152287. The genetic results support the distinctiveness of the two In view of these results we formally re-instate the name C. species C. erythrocephala (= C. erythrostoma) and C. eryth- erythrosoma to species rank. Additionally, following the dis- rosoma, as suggested by Pujade-Villar et al. (2005), although cussion presented by Pujade-Villar et al. (2005), the sexual they are each other’s closest relative (Figure 1). Variation form of C. erythrocephala corresponds to the species origi- between sympatric individuals of the two species averaged nally described as C. hartigi whereas the sexual form of C. 2.4% (see Table 1), a value comparable to between-species erythrosoma is the morphologically distinct but as yet unde- variation both in other cynipid species (Nicholls et al. 2012; scribed generation illustrated in Figure 4 of Pujade-Villar et Cerasa et al. 2018; Nicholls et al. 2018) and among al. (2005). We note as well that these two sexual forms differ

Table 1. Pairwise genetic distances among the four Callirhytis species present in Europe and known from their asexual generations, based upon 433 base pairs of the cytochrome b gene using a HKY correction. Values on the diagonal indicate average percentage variation among individuals of the same species; off-diagonal values indicate between-species distances

C. erythrosoma C. erythrocephala C. rufescens C. glandium

C. erythrosoma 0.5 — — — C. erythrocephala 2.4 0.0 — — C. rufescens 5.3 5.1 0.0 — C. glandium 5.3 4.6 4.1 0.0

Butlletí ICHN 84, 2020 Re-instatement of the species name Callirhytis erythrosoma (Dettmer, 1933) 33 NOTA BREU to a greater extent than the recognised species pair of C. bella diameter of a ocellus) and transfacial line much shorter and C. glandium. than the height of a compound eye...... C. rufescens – Predominantly reddish-brown colour. Notauli incomplete, To identify the European species (both sexual and asexual invisible on the anterior third of the mesoscutum. Radial forms) we establish the following key: cell longer (about 3.7 times longer than wide). Males with relatively smaller ocelli (OOL 0.9-1.2 times as long as 1 Asexual females; robust specimens (body length 2.5-3.0 the diameter of the lateral eye) and transfacial line almost mm). Gena strongly broadened behind eye; head trans- equal to the height of a compound eye...... 7 verse, dull rugose; scutum with strong transverse irregu- 7 Head around 2.0 times as broad as long in dorsal view. lar striae; galls exclusively in acorns on oaks belonging Scutellar foveae separated by a wide central area. Females to Quercus section Cerris (Q. cerris, Q. suber, Q. ilex, Q. POL 1.5-1.6 times as long as OOL and F1 3.0 times as macrolepis and occasionally Q. coccifera)...... 2 long as broad. Males with notauli reaching 2/3 the length – Sexual females and males; non-robust specimens (body at of the mesoscutum and OOL shorter than diameter of lat- most 2.5 mm). Gena slightly broadened behind eye; head eral ocellus...... C. erythrocephala rounded or taller than broad in front view, coriaceous, – Head broader, less transverse. Scutellar foveae separated with less dull sculpture; scutum with more delicate trans- by a point or a little carina. Females POL subequal to OOL verse striae; galls in twigs or buds on oaks of Quercus and F1 around 2.1 times as long as broad. Males with no- section Quercus (Q. faginea, Q. pubescens, Q. pyrenaica, tauli reaching 1/3 the length of the mesoscutum and OOL Q. robur, among others)...... 5 slightly longer than diameter of lateral ocellus...... 2 Tarsal claws with basal lobe. Radial cell 3.0 times as long ...... C. erythrosoma as broad; 2nd abscissa of radius slightly curved. Scutum with strong transverse regular striae. Body almost com- Finally, we provide comment on the status of one further pletely black or dark reddish brown...... C. glandium Callirhytis species, C. cameroni, a species known from leaf – Tarsal claws simple or with very weak basal lobe. Radial galls on Q. salicifolia (Quercus section Lobatae) in Panama cell longer, 3.5 times as long as broad; 2nd abscissa of (Medianero & Nieves-Aldrey 2014). As with most other Ne- radius nearly straight. Scutum with less strong transverse arctic Callirhytis, it lacks the diagnostic characters of Cal- striae, usually irregular, waved and/or with anastomoses lirhytis «sensu stricto»; it is currently classified asCallirhytis in posterior 1/2-1/3. Body colour variable, from almost «sensu lato» only based on the apparently incorrect charac- entirely reddish yellow to predominantly black...... 3 ters of Weld (1952). According to the original description, C. cameroni has reticulate sculpture on the third and follow- 3 Body yellow-red to amber. Frons and vertex microretic- ing metasomal tergites, and such sculpturing never occurs in ulate, without strong branched striae. Notauli complete, Callirhytis «sensu stricto». Reticulate or strongly alveolate sometimes less distinct in anterior 1/3. Scutum with less metasomal sculpturing is rare in Nearctic and only marked regular transverse striae. Tarsal claws simple. occurs in the genus Melikaiella Pujade-Villar, 2014. Calli- Galls on Q. suber and Q. ilex...... C. rufescens rhytis cameroni also shares other characters typical of Me- – Body predominantly black or completely yellow-red. likaiella (see Pujade-Villar et al., 2014): lower facial carinae Frons and vertex dull rugose with strong striae. Notauli present only along the malar sulcus (carinae radiating from incomplete, invisible in anterior 1/3. Scutum with strong clypeus present in the entire malar area and extending on the transverse waved, irregular rugae, with anastomoses pos- lower face up to toruli in Callirhytis), a very strong irregular teriorly. Tarsal claws without or with very weak basal rugose sculpture on mesoscutum (not transversely carinated lobe. Galls on Q. cerris...... 4 as in Callirhytis) with coriaceous interspaces (interspaces 4 Mesosoma completely black. OOL subequal to LOL. Ver- smooth and shiny in Callirhytis), circumscutelar carina (ab- tex with strong rugae, inter-ocellar area always with lin- sent in Callirhytis) and mesopleuron having coriaceus reticu- ear elements...... C. erythrocephala late sculpture (with transverse and interrupted striae in Cal- – Mesosoma red-yellowish. OOL longer than LOL. Vertex lirhytis). The host plant of C. cameroni occurs on Quercus coriaceous sometimes with weak rugae, inter-ocellar area section Lobatae section as is the case with other Melikaiella occasionally with linear elements...... C. erythrosoma species (sections Quercus and Cerris are hosts of true Cal- lirhytis). Accordingly, we transfer C. cameroni to the genus 5 Tarsal claws toothed, with an acute basal lobe...... Melikaiella, with the new name Melikaiella cameroni (Medi- ...... C. bella and C. glandium anero & Nieves-Aldrey, 2014) n. comb. [C. bella emerge from inconspicuous bud galls and C. glandium from twigs] – Tarsal claws simple or with blunt basal lobe...... 6 Acknowledgements 6 Body with amber colour. Notauli complete, sometimes weakly impressed on the anterior part of the mesoscu- We thank François Barbotin(†), José Luis Nieves-Aldrey, tum. Radial cell relatively short (3.1-3.3 times longer than György Csóka and Simon Haarder for providing some of the wide). Males with large ocelli (OOL equal to 0.5 times the specimens sequenced in this study. Also we thank George

Butlletí ICHN 84, 2020 34 J. A. NICHOLLS & J. PUJADE-VILLAR NOTA BREU

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