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Description and biological features of a new species of Anagrus Haliday ( Hymenoptera , Mymaridae )

Anagrus lindberginae sp. n. (Hymenoptera: Mymaridae), an egg parasitoid of the leafhopper Lindbergina aurovittata (Homoptera: Cicadellidae), is described from Italy. It is included in the atomus group of Anagrus Haliday and compared with the allied known taxa. The parasitoid’s life cycle is characterized by a long larval diapause from spring to fall, which allows for synchronization with its leafhopper host; other biological traits of A. lindberginae on the evergreen plant Quercus ilex are discussed. Introduction Some years ago, one of the authors (G.V.) started to study egg parasitoids of leafhoppers (Cicadellidae), mostly in southern Italy. Efforts were made to collect members of Anagrus Haliday (Hymenoptera: Mymaridae) from wild and cultivated host plants, and possibly from known insect hosts. Most of the collected species belonged to the atomus species group as defined by Chiappini (1989). Their morphology and phenology were studied in relation to some agroecosystems (Viggiani, 1991; 2009; Viggiani et al., 2003; 2004a; 2004b; Viggiani & Jesu, 2005; Matteucig & Viggiani, 2008; Velocci & Viggiani, 2008). Taxonomic discrimination of A. atomus (Linnaeus) and A. ustulatus Haliday (sensu Chiappini, 1989) was not confirmed by molecular analysis of ITS2 and COI, but in this complex a clade corresponding to Anagrus ustulatus from eggs of Lindbergina aurovittata (Douglas) on Quercus ilex L. was clearly distinct (Monti et al., 2009). This evidence suggested a more in-depth morphological analysis and molecular characterization, integrated with extensive biological data (Nugnes, 2011; Nugnes et al., 2011). In this paper the Anagrus species reared from L. aurovittata on Q. ilex is recognized and described as a new species belonging to the atomus species group. Anagrus presently includes 92 valid species (Noyes, 2013); only 19 of them are included in the atomus species group of A. (Anagrus Haliday). The atomus group was defined in different ways (Graham, 1982; Chiappini, 1989; Chiappini et al., 1996), but the main discriminating character is the presence of only 3 multiporous plate sensilla (mps) on the antennal club of females. Materials and Methods Leaves of Q. ilex were randomly collected in several locations of Campania (mostly in Portici, NA, and in Vietri sul Mare, SA) and in Basilicata (Rivello, PZ). In the laboratory the parasitised eggs of L. aurovittata were individually isolated with a small piece of leaf tissue in a microcapsule (diameter 15 and height 15 mm). The leafhopper host was previously identified according to features of the male genitalia, as illustrated by Vidano et al. (1990). Emerged parasitoids of Anagrus were slide-mounted in Canada balsam phenol. Samples of specimens caught by sticky yellow traps, placed in the Q. ilex woodland of Parco Gussone (Portici), from October 2011 to June 2013, were also slide-mounted. All the material was examined under a Zeiss Axiophot microscope and measurements were taken and given in μm. Terminology used in this article follows Gibson (1997), Huber (2012) and Debauche (1948) for forewing macrosetae. From December 2009 to April 2010, 3 yellow sticky traps (Glutor, SYSTEMATICS AND PHYLOGENY Description and biological features of a new species of Anagrus Haliday (Hymenoptera, Mymaridae) F. Nugnes, G. Viggiani Laboratorio di Lotta Biologica, Dipartimento di Agraria, Università di Napoli Federico II, Portici, Italy Correspondence: Gennaro Viggiani, Laboratorio di Lotta Biologica, Dipartimento di Agraria, Università degli Studi di Napoli Federico II, Via Università 133, Portici (NA), Italy E-mail: genviggi@unina.it


Introduction
Some years ago, one of the authors (G.V.) started to study egg parasitoids of leafhoppers (Cicadellidae), mostly in southern Italy. Efforts were made to collect members of Anagrus Haliday (Hymenoptera: Mymaridae) from wild and cultivated host plants, and possibly from known insect hosts. Most of the collected species belonged to the atomus species group as defined by Chiappini (1989). Their morphology and phenology were studied in relation to some agroecosystems (Viggiani, 1991;2009;Viggiani et al., 2003;2004a;2004b;Viggiani & Jesu, 2005;Velocci & Viggiani, 2008). Taxonomic discrimination of A. atomus (Linnaeus) and A. ustulatus Haliday (sensu Chiappini, 1989) was not confirmed by molecular analysis of ITS2 and COI, but in this complex a clade corresponding to Anagrus ustulatus from eggs of Lindbergina aurovittata (Douglas) on Quercus ilex L. was clearly distinct (Monti et al., 2009). This evidence suggested a more in-depth morphological analysis and molecular characterization, integrated with extensive biological data (Nugnes, 2011;Nugnes et al., 2011). In this paper the Anagrus species reared from L. aurovittata on Q. ilex is recognized and described as a new species belonging to the atomus species group.
Anagrus presently includes 92 valid species (Noyes, 2013); only 19 of them are included in the atomus species group of A. (Anagrus Haliday). The atomus group was defined in different ways (Graham, 1982;Chiappini, 1989;Chiappini et al., 1996), but the main discriminating character is the presence of only 3 multiporous plate sensilla (mps) on the antennal club of females.

Materials and Methods
Leaves of Q. ilex were randomly collected in several locations of Campania (mostly in Portici, NA, and in Vietri sul Mare, SA) and in Basilicata (Rivello, PZ). In the laboratory the parasitised eggs of L. aurovittata were individually isolated with a small piece of leaf tissue in a microcapsule (diameter 15 and height 15 mm). The leafhopper host was previously identified according to features of the male genitalia, as illustrated by Vidano et al. (1990). Emerged parasitoids of Anagrus were slide-mounted in Canada balsam phenol. Samples of specimens caught by sticky yellow traps, placed in the Q. ilex woodland of Parco Gussone (Portici), from October 2011 to June 2013, were also slide-mounted. All the material was examined under a Zeiss Axiophot microscope and measurements were taken and given in µm. Terminology used in this article follows Gibson (1997), Huber (2012) and Debauche (1948)  13×24 cm) were installed at a distance of about 30 m from each other in a Q. ilex woodland at Portici (50 m elevation) and removed every two weeks. From October 2011 to June 2013 traps of the same type were placed in the same area, but removed weekly. In the laboratory each trap was examined, the adults of Anagrus and those of L. aurovittata were recorded. Samples of 100 Q. ilex leaves were taken at random each week in the same woodland from November 2009 to April 2010. On each leaf the eggs (healthy and parasitised) and the young stages of L. aurovittata were recorded. Two samples, each of 50 leaves, were randomly taken on 2.x.2009 and 11.iii.2011 for evaluation of degree of infestation by L. aurovittata and the percentage parasitism of their eggs by Anagrus.
Adult emergence of Anagrus and L. aurovittata in the field was also followed by marking some eggs on Q. ilex leaves and examining them weekly.
ETYMOLOGY. The specific name lindberginae refers to the leafhopper host genus.
DISTRIBUTION. The new species is recorded from Campania, Liguria and Piedmont in Italy. The A. atomus referred by Bosco & Arzone (1991) as parasitoid of Lindbergina spp. is to be considered A. lindberginae (voucher specimens examined by G.V.).
REMARKS. In the key to Holarctic species of Anagrus (Chiappini et al., 1996), A. lindberginae goes to the same couplet as A. longitibialis Donev, the only other known European species that has the same ovipositor/fore tibia ratio (1.5-1.6), but A. longitibialis differs by having a mps on both F3 and F4. However, it is A. ustulatus sensu Chiappini that the new species resembles the most. It differs morphologically from this species by the ratios ovipositor length/fore tibia and ovipositor length/third valvula.
The most common species of the A. atomus group allied to A. lindberginae are A. atomus and A. ustulatus (sensu Chiappini, 1989). Morphometric data on females of these Anagrus species were given by Chiappini (1987). According to Chiappini et al. (1996) females of A. atomus can be distinguished by the following combination of features: club with three mps, F3 without mps, F4 with one mps; ovipositor/fore tibia ratio about 2.0; mesoscutum without setae; forewing with three irregular rows of discal hairs in basal half, and three or four rows anterior to hairless area, hairless area at broadest part of forewing short, FWL/FWW <10. In the description of the neotype of A. atomus, Chiappini & Triapitsyn (2007) add other characters to the diagnosis of A. atomus: F2 a little longer than F3; club a little longer than two preceding segments combined; forewing 6.8 times as long as wide; distal macrochaeta about 2.5 times the length of the proximal macrochaeta.
Anagrus ustulatus Haliday (1833, p. 347) was described as follows: Sp. 3. A. ustulatus. Fuscus antennis thoracis disco pedibusque ferrugineis, alis hyalinis. ♂ (Long. 0.03; alar. 0.08.). Precedentibus brevior, colore obscuriore; alae ut in A. atomo. Graham (1982, p. 201) stated that of the seven specimens that stand under this name in Haliday's collection, but all except the first two (Nos. 70 and 71) are females. No 70 agrees with the original description and is now designed LECTOTYPE. He stated that the females were clearly conspecific with the male lectotype and did not accept the synonymy of A. ustulatus with A. atomus proposed by Debauche (1948). In his key Graham (1982, p. 198) stated that ustulatus shows forewing very broad for the genus 5.7-6.1 times as long as broad and with 8-9 longitudinal rows of hairs in its distal part. Chiappini (1989) recognised that her Anagrus sp. obtained from leafhoppers on bramble and rose is conspecific with A. ustulatus. However, that species does not fit with the characters given by Graham in his key. In A. ustulatus sensu Chiappini the ratio of forewing length/forewing width is 8.237 (9.400-7.200) and the rows of hairs on the discal area are 4-5. But according to Graham (1982, p. 201) the genitalia of the lectotype male of ustulatus are unlike those of atomus but similar to the type found in the incarnatus species-group; according to Chiappini (1989, p. 104) the genitalia of A. ustulatus are typical of atomus group. That does not help to characterize the species properly. The situation is worse for the female of A. ustulatus, which Graham (1982) considered a species sola and did not include in the atomus speciesgroup. In fact, of the 5 female specimens standing under this name in Haliday collection the two numbered 72 and 73 belong to A. incarnatus Haliday (Chiappini and Triapitsyn, 2007). In conclusion, the validity of A. ustulatus Haliday remains uncertain. For an attempt at clarification the genitalia of the male lectotype and all females under this name in Haliday's collection need to be properly slide-mounted and studied. One of the present authors (G.V.) is doing this.
Our morphometric data (Tables 1-3) on several populations of A. atomus and A. ustulatus sensu Chiappini show that morphological discrimination of the female may be substantially based only on the presence or absence of a sensory ridge on F4; intermediate forms are rather rare. The other characters reported by Chiappini and Triapitsyn (2007) (ratio of F2/F3; ratio of club length/F5+F6 length; ratio of forewing length/forewing width; ratio of distal macrochaeta length/proximal macrochaeta length; number of hair rows on forewing disc, extension of hairless area at broadest part of forewing; ovipositor/fore tibia ratio) are widely variable and overlapping.
Very limited information is available about the morphological characters of males of the atomus group. Some measurements on the male genitalia are reported by Chiappini and Mazzoni (2000) and Floreani et al. (2006). They show no significant differences for distinguishing A.  Soyka (1955). At present Anagrus ustulatus Haliday 1833, based on a lectotype male, revised by Graham (1982) and Chiappini (1989), can not be definitely linked to any female species of the atomus group of Anagrus.

Host and parasitoid ecology
In Italy, the leafhopper L. aurovittata overwinters as an egg in the leaf of the evergreen plants Q. ilex, Q. suber (Vidano et al, 1990), M. communis and R. ulmifolius (Viggiani et al., 2004b;Matteucig and Viggiani, 2008), but also as an adult, as recorded below (Figures 2-4). The most common winter host of L. aurovittata, at least in Campania, is Q. ilex. During spring the species completes one generation and new adults leave the winter hosts and spread to plants with deciduous leaves such as some Quercus spp. and Castanea spp. (Viggiani, 1991;2009). From summer to late autumn the leafhopper can complete more generations. The leafhopper adults then go back on the overwintering hosts and oviposit in subepidermic slits on the leaves, normally by laying single eggs.
The parasitoid Anagrus lindberginae shows a long diapause as a young larva in the host egg ( Figure 5), starting from March-April.
From October-November ( Figure 6) this stage completes its development in a pupa followed by the adult emergence. These phenological stages of A. lindberginae are synchronized with the presence of host Article     new eggs. The parasitoid oviposits in the progressively available host eggs and their young stages develop during winter, when most of the adults emerge (Figures 2-4). They can oviposit in the remaining, left over healthy host eggs, but most of their progeny will start a long diapause period as young larvae from spring to fall. Anagrus lindberginae completes at least one generation from late autumn to early spring. Over several years it has been confirmed that the population of A. lindberginae is represented almost exclusively by females; males are very rare (Viggiani et al., 2003). In the woodland of Parco Gussone (Portici) the percentage of Q. ilex leaves with eggs of L. aurovittata ranged from 66-54% ( Figure 7); that of the not-parasitised eggs varies from 6.5-37.3%.

Discussion and Conclusions
The concept of the atomus group has changed somewhat (Chiappini, 1989;Chiappini et al., 1996;Chiappini & Mazzoni, 2000). At present this group includes species with 3 mps on the antennal club of females and the genitalia of males, with digiti spines straight or bent. Among the Holarctic species of Anagrus, only 8 species are included in the atomus group. The genotype species, A. atomus, is widespread and rather well characterized (Chiappini & Triapitsyn, 2007), but the identity of the allied species A. ustulatus still remains questionable for the following reasons: i) the poor original description is based on a male, which was designed lectotype (Graham, 1982); ii) no female in the Haliday collection can be definitely associated with the lectotype male; in fact some specimens considered clearly conspecific by Graham (1982) belong to A. incarnatus (Chiappini & Triapitsyn 2007); iii) the interpretation of A. ustulatus given by Chiappini (1989) is uncertain; iv) the very small morphological differences between A. atomus and A. ustulatus sensu Chiappini (presence or absence of a mps on F4) are not supported by the molecular data (Monti et al., 2009). However Cargnus & Pavan (2007 have found enzymatic differences between females of A. atomus and A. ustulatus reared from the leafhoppers on bramble and grape. Floreani et al. (2006), using the cuticular hydrocarbon analysis, found two distinct profiles for A. atomus and A. ustulatus, classified according to the morphological characters given by Chiappini (1989).
The new species A. lindberginae appears morphologically clearly distinguishable among the atomus group species, supported by the molecular data (Monti et al., 2009;Nugnes, 2011). As in a few other species or populations of Anagrus, A. atomus (MacGill, 1934;Choudhury & Copland 2003), A. delicatus (Cronin & Strong, 1996), and A. takeyanus (Chiappini et al., 1996), the reproduction of A. lindberginae takes place through thelytokous females. The life cycle is well syncronized with that of the host.
In the system Q. ilex -L. aurovittata -A. lindberginae two main biological phenomena are involved: migration and diapause. The leafhopper migration in spring from the evergreen hosts to plants with deciduous leaves for reproduction during summer and autumn avoids unfavorable conditions. The larval diapause of A. lindberginae allows the parasitoid to survive during a long period in its host's absence. At present, parasitised eggs of L. aurovittata by A. lindberginae were not recorded in any of the known deciduous host plants of this leafhopper.
A similar case was reported by Tsukada (1999). In Japan, the andromeda lace bug Stephanitis takeyai Drake et Maa (Heteroptera: Tingidae), shows a seasonal host-plant alternation between its main host plants, the evergreen Pieris japonica and the deciduous Lyonia ovalifolia. In some sites where the latter host is rare, the tingid reproduces on P. japonica all year around. The seasonal alternative host for S. takeyai seems derived from the ancestral non-alternating life cycle. In places were the insect host develop only one generation a year, the egg parasitoid of the tingid, Anagrus takeyanus Gordh and Dunbar, enters in a summer diapause.