Conidarnes, a new oriental genus of Sycophaginae (Hymenoptera, Agaonidae) associated with Ficus section Conosycea (Moraceae)

Abstract The sycophagines are strictly associated with two subgenera of Ficus L. (Moraceae), namely Sycomorus and Urostigma. They mostly oviposit through the fig wall and lay their eggs within the fig flowers, being either gall-makers or parasitoids of other fig wasps. In this contribution, a new genus of Sycophaginae, Conidarnes Farache & Rasplus, gen. n., is described with seven new species: Conidarnes achterbergi Farache & Rasplus, sp. n.; Conidarnes bergi Farache & Rasplus, sp. n.; Conidarnes laevis Farache & Rasplus, sp. n.; Conidarnes santineloi Farache & Rasplus, sp. n.; Conidarnes subtectae Farache & Rasplus, sp. n.; Conidarnes sulcata Farache & Rasplus, sp. n.; and Conidarnes sumatranae Farache & Rasplus, sp. n. Illustrations, morphological diagnoses, dichotomous keys and multi-entry online keys to species are provided. Conidarnes species strictly occur in the oriental region, and their distribution does not overlap with the distribution of the two other genera belonging to the same clade. Due to their relative rarity, we encourage extensive sampling of Conosycea figs to improve our knowledge of the genus.


Introduction
Recent phylogenetic analyses of the Chalcidoidea have retrieved Sycophaginae as sister to the pollinating Agaoninae (Heraty et al. 2013). Consequently, the family Agaonidae is now subdivided into two subfamilies: the Agaoninae and the Sycophaginae. The Agaoninae have established a very specialized relationship with Ficus L. (Moraceae) (Cook and Rasplus 2003). These wasps are the main pollinators of fig trees and are capable of entering the fig inflorescences through a small pore, called the ostiole. Once inside the figs, these wasps pollinate and lay their eggs in some pistilate flowers (Galil and Eisikowitch 1968 (Bouček 1988;Cruaud et al. 2011b;Elias et al. 2008). A few species (a small species-group of Afrotropical Sycophaga Westwood, Cruaud et al. 2011b) enter the fig through the ostiole (Galil et al. 1970).
There are about 60 described species of Sycophaginae that occur in all tropical and subtropical regions. The subfamily Sycophaginae was retrieved as a monophyletic assemblage and divided into three main clades each of which may warrant tribal status (Cruaud et al. 2011a): 1) A first clade-sister to the remaining Sycophaginae-that only includes Eukoebelea Ashmead species associated with Ficus subsection Malvanthera in Australasia. 2) A clade that includes species of large and early gallmakers, belonging to three genera: i) the Australasian genus Pseudidarnes Girault associated with Ficus subsection Malvanthera, ii) the Neotropical Anidarnes Bouček associated with Ficus section Americana, and iii) a few species associated with Ficus section Conosycea that cannot be placed in any existing genus which requires the establishment of the new genus described here. 3) Sister to the previous clade, a highly diversified clade composed of the New World Idarnes Walker associated with Ficus section Americana, and the Old World Sycophaga mostly associated with Ficus subgenus Sycomorus, but also including two species associated with Ficus subgenus Urostigma section Urostigma.
We have recently reviewed the genera Anidarnes and Pseudidarnes with the description of nine new Anidarnes and six new Pseudidarnes species (Farache et al. 2013;Farache and Rasplus 2014). In this paper, we propose the establishment of Conidarnes, a new oriental genus of Sycophaginae, and describe seven new species mostly sampled from figs of the large strangling fig trees (Conosycea) that occur in the dipterocarp rainforests of the oriental region. We also provide illustrations, morphological diagnoses, dichotomous keys, and multi-entry online keys to species.

Methods
Specimen handling and imaging follow Farache and Rasplus (2014). Geographical coordinates and altitudes were mostly estimated using label information. Morphological terminology follows Gibson (1997), and the HAO (Hymenoptera Anatomy Ontology) portal (Yoder et al. 2010). Species descriptions were assembled in DELTA (Dallwitz 1980). A list of characters and character states used to describe the species can be found in Suppl. material 1. Characters included in this list were matched with HAO portal codes. This may help readers to better understand the anatomical structures we used for description. The sections dealing with the material examined were prepared using AUTOMATEX (Brown 2013). Multi-entry identification keys were built using LUCID®, and are available at http://www.figweb.org.
Images were produced with a Leica M16 lens and a JVC KY-75U 3CCD digital camera. Cartograph v5.6.0 (Microvision, Evry, France) software was used for focus stacking.
Type and specimen depositories, and their respective curators are:  Diagnosis. Antennae with 13-14 antennomeres (one or two anelli), including a stub or nipple-like terminal flagellomere. Funicular segments slightly longer than wide to transverse. Antennae inserted at the middle line of compound eyes or below. Toruli contiguous. Clypeal margin bilobed. Malar sulcus absent. Petiole very short, transverse. Ovipositor sheaths without a median constriction and depigmentation.

Conidarnes
Generic description. Females. Size and colour. Body length 1.5-4.0 mm. Length of the ovipositor sheaths 0.4-6.4 mm. Body colour variable. Antennae mostly yellow, sometimes with orange or brown tinges. Head and mesosoma brown to black, usually with green, blue and orange metallic lustre. Legs yellow to brown. Coxae sometimes concolorous with mesosoma. Wings hyaline, sometimes medially infuscate in males. Metasoma usually brown black, sometimes yellow.
Head. Antenna with 13 or 14 antennomeres (including a stub or nipple-like terminal antennomere), usually with two anelli but sometimes with a single anellus (antennal formula 11263 or 11163). Terminal antennomere (i.e. a nipple-like thirteenth or fourteenth antennomere) sometimes conspicuous. Funicular segments slightly longer than wide to transverse. Face sculpture usually reticulate, sometimes slightly engraved. Upper face sometimes smooth. Antennae inserted at the middle line of compound eyes or below. Toruli contiguous, distance between toruli always smaller than one torulus diameter. Clypeal margin bilobed. Malar sulcus absent.
Metasoma. Petiolate, petiole very short, transverse. Margin of eighth gastral tergite deeply sinuate, A-like, with thumbnail-like medial flap (epipygium) and with a peglike cercus arising from the membrane on either side of the epipygium (apomorphy of Sycophaginae). Length of the ovipositor sheaths varying from 0.3× (about as long as the hind tibia) to nearly twice as long as body. Ovipositor sheaths without a median constriction and depigmentation.
Males. Similar to females but usually slender and shorter. Exhibiting different coloration, the mesosoma sometimes mostly yellow. Wings sometimes medially infuscate.
Etymology. The generic name is masculine and derived from Idarnes Walker, 1843, in the same manner than other sycophagine genera (Pseudidarnes Girault, 1927 andAnidarnes Bouček, 1993) and is associated to the prefix Con used for Conosycea, the host plant section of the included species. The origins of the name Idarnes were discussed in Farache et al. (2013).

1
Notauli incomplete (Fig. 6D). Upper face smooth and lower face reticulate (Fig. 6C) Sculpture of mesoscutum and mesoscutellum mostly smooth, lateral lobes of mesoscutum engraved reticulate (Fig. 12D). Scrobe with a median longitudinal sulcus, extending from median ocellus to interantennal area (Fig. 12C) Antennae inserted near the middle line of compound eyes (Fig. 14C). Supraclypeal area higher than clypeus (Fig. 14C). Propodeum with a reticulate median line, slightly striate, and wider near the anterior margin of the propodeum ( Description. Female. Size and colour. Body length 3.8 mm. Length of the ovipositor sheaths 6.4 mm. Antennae yellow orange. Head and mesosoma with metallic lustre, mostly green and blue. Head dorsally more orange. Legs yellow. Metasoma ventrally yellow, dorsally dark brown.
Head. Scape 4.8× as long as wide. Antenna with two anelli. Proximal anellus longer than distal anellus. Funicular segments mostly as long as wide or slightly longer than wide. Terminal antennomere conspicuous. Antennae inserted at the lower line of compound eyes. Supraclypeal area shorter than clypeus and narrow. Face sculpture reticulate. Scrobe without a median longitudinal sulcus.

Male. Unknown.
Etymology. The species is dedicated to our colleague and renowned specialist of Hymenoptera, Kees van Achterberg who collected the holotype.
Biology. Unknown    Description. Female. Size and colour Body length 2.8 mm. Length of the ovipositor sheaths 1.3 mm. Head and mesosoma black, slightly green. Metallic lustre faint. Antennae and legs yellow, coxae concolorous with mesosoma. Metasoma brown.

Conidarnes bergi
Head. Scape 5× as long as wide. Antenna with two anelli. Proximal anellus longer than distal anellus. Funicular segments mostly as long as wide or slightly longer than wide. Terminal antennomere inconspicuous. Antennae inserted at the lower line of compound eyes. Supraclypeal area shorter than clypeus, narrow. Face sculpture reticulate. Scrobe without a median longitudinal sulcus.
Male. Similar to female, except the following characters: Head and mesosoma darker. Legs browner. Pedicel and funicular segments more elongated. Antenna more setose. Pronotum more elongated. Biology. Reared from syconia of Ficus involucrata Blume.   Mesosoma. Pronotum sculpture mostly smooth, slightly engraved. Pronotum elongated, nearly twice as long as high in lateral view. Mesoscutum and mesoscutellum sculpture mostly smooth. Notauli incomplete. Frenal sulcus smooth. Metascutellum short, inconspicuous. Anterior margin of propodeum smooth. Propodeum sculpture smooth. Propodeum without a median line.

Male. Unknown.
Etymology. The specific name refers to the smooth body sculpture observed in this species.
Note. This species presents unique characters, such as a smooth body with no sculpture and an elongated mesosoma. These characters are mostly associated to galler fig wasps that enters the syconium through the ostiole (Cruaud et al. 2011b). Consequently, we speculate that this species may be an ostiolar galler.   Description. Female. Size and colour. Body length 1.6 mm. Length of the ovipositor sheaths 0.45 mm. Head, mesosoma, and metasoma black, slightly green. Metallic lustre faint. Antennae and legs yellow, forecoxae brown.

Conidarnes santineloi
Head. Scape 3.5× as long as wide. Antenna with one anellus. Funicular segments mostly transverse. Terminal antennomere inconspicuous. Antennae inserted just below the middle line of compound eyes. Supraclypeal area higher than clypeus, wide. Face sculpture reticulate. Scrobe without a median longitudinal sulcus.
Etymology. The specific name is dedicated to our friend and colleague Rodrigo Augusto Santinelo Pereira due to his excellent and pioneering work on fig wasps and Ficus in Brazil.
Biology. Collected from syconia of Ficus pallescens L., the form with small leaves (see Berg and Corner 2005). Diagnosis. Antenna with two anelli. Funicular segments mostly as long as wide or slightly longer than wide. Antennae inserted just below the middle line of compound eyes. Supraclypeal area wide. Mesoscutum and mesoscutellum reticulate. Length of the ovipositor sheaths 0.9× body length.

Conidarnes subtectae
Description. Female. Size and colour. Body length 1.8 mm. Length of the ovipositor sheaths 1.6 mm. Antennae yellow. Head and mesosoma black, with faint blue, green, and orange metallic lustre. Legs mostly yellow distally. Coxae almost concolorous with body. Femora yellow brown. Metasoma dark brown.
Head. Scape 4.8× as long as wide. Antenna with two anelli. Proximal anellus longer than distal anellus. Funicular segments mostly as long as wide or slightly longer than wide. Terminal antennomere conspicuous. Antennae inserted just below the middle line of compound eyes. Supraclypeal area higher than clypeus, and wide. Face sculpture reticulate. Scrobe without a median longitudinal sulcus.
Mesosoma  Diagnosis. Scrobe with a median longitudinal sulcus, extending from median ocellus to interantennal area. Mesoscutum and mesoscutellum sculpture mostly smooth. Lateral area of the mesoscutum mostly engraved reticulate. Propodeum sculpture smooth, slightly engraved alutaceous near spiracles. Propodeum without a median line. Length of the ovipositor sheaths 1× body length.
Description. Female. Size and colour. Body length 2.7 mm. Length of the ovipositor sheaths 2.6 mm. Antennae yellow. Head with metallic lustre, mostly green, slightly orange and blue. Mesosoma mostly brown, with faint metallic lustre, green and blue. Legs mostly brown, tarsal segments and foretibia yellow. Metasoma dark brown.
Head. Scape 4.6× as long as wide. Antenna with two anelli. Proximal anellus nearly as long as distal anellus. Funicular segments mostly transverse. Terminal antennomere conspicuous. Antennae inserted at the lower line of compound eyes. Supraclypeal area inconspicuous. Face sculpture mostly reticulate, smooth near scrobe. Scrobe with a median longitudinal sulcus, extending from median ocellus to interantennal area. Mesosoma. Pronotum sculpture alutaceous, engraved. Pronotum elongated, nearly twice as long as high in lateral view. Prosternal posterior margin medially acute. Mesoscutum and mesoscutellum sculpture mostly smooth. Lateral area of the mesoscutum mostly engraved reticulate. Notauli complete. Frenal sulcus smooth. Metascutellum as long as frenum, smooth, and not well delimited laterally. Anterior margin of propodeum smooth. Propodeum sculpture smooth, slightly engraved alutaceous near spiracles. Propodeum without a median line. Metasoma. Length of the ovipositor sheaths 1× body length. Male. Similar to female except the following characters: Mesosoma and metasoma mostly yellow. Axillulae, metanotum, and propodeum mostly brown. Some metasomal segments slightly brown dorsally. Scape and pedicel shorter, funicular segments more transverse. Antenna more setose.
Etymology. The specific name refers to the longitudinal sulcus separating the scrobal cavity in this species.

Conidarnes sumatranae
Diagnosis. Antennae inserted near the middle line of compound eyes. Funicular segments mostly as long as wide or slightly longer than wide. Mesoscutum and mesoscutellum sculpture reticulate. Propodeum with a reticulate median line, slightly striate, and thicker near anterior margin. Length of the ovipositor sheaths 0.4× body length.
Description. Female. Size and colour. Body length 1.9 mm. Length of the ovipositor sheaths 0.8 mm. Antennae yellow. Head and mesosoma black, with green and blue metallic lustre. Legs mostly yellow, forecoxae concolorous with body. Hindcoxae proximally concolorous with body. Metasoma dark brown.
Head. Scape 3.5× as long as wide. Antenna with two anelli. Proximal anellus longer than distal anellus. Funicular segments mostly as long as wide or slightly longer than wide. Terminal antennomere inconspicuous. Antennae inserted near the middle line of compound eyes. Supraclypeal area higher than clypeus and narrow. Face sculpture reticulate. Scrobe without a median longitudinal sulcus.

Comments.
We have examined only males, but they clearly belong to an undescribed species. Since we described Conidarnes species mostly based on females, we prefer not to describe this species until more specimens are found.

Discussion
In this study, we describe a new oriental genus of Sycophaginae that includes seven new species. Conidarnes can easily be assigned to Sycophaginae due to the presence of a square mesoscutellum and the morphology of the terminal gastral tergites/epipygium, which are synapomorphies of the subfamily (Cruaud et al. 2011b;Rasplus and Soldati 2005). The assignment of Conidarnes to Sycophaginae is also corroborated by previous phylogenetic analyses (Cruaud et al. 2011a;Cruaud et al. 2011b). Among the Sycophaginae, Conidarnes is uniquely defined by the following combination of characters: toruli contiguous; antennae inserted at, or below, the median line of compound eyes; malar sulcus absent; petiole very short, transverse.
Phylogenetically, Conidarnes is nested within a clade including Pseudidarnes and Anidarnes. Species belonging to this clade are large gall inducers (Cruaud et al. 2011b). This biology seems to be shared by all members of the clade, a life-history strategy that is also found in the Idarnes incertus species group and in a few Sycophaga species (Cruaud et al. 2011b). Large gall inducers oviposit early during fig development, species are overall larger and have shorter ovipositors than the other Sycophaginae species developing in the same fig (Cruaud et al. 2011b). Based on morphology and phylogenetic relationships, most Conidarnes species seem to be large gall-inducers, which oviposit through the syconium wall several days before pollination, though this still needs to be confirmed by behavioural observations. One peculiar species, Conidarnes laevis, exhibits a rather flattened and smooth body (Figs 6A, E). Such morphology may indicate that females enter the fig through the ostiole. If this biology is confirmed by field observations, it would be a second independent case of an ostiolar Sycophaginae besides species of the Sycophaga sycomori species group that are associated with Ficus subgenus Sycomorus in the Afrotropical region (Galil et al. 1970).
Conidarnes species are restricted to the Oriental region. Only one species was sampled in continental Asia (C. sulcata, from Xishuangbanna in southwest China), whereas all other species were sampled in the insular region of Southeast Asia: five species in Borneo (C. achterbergi, C. laevis, C. santineloi, C. subtectae, and an undescribed species ex Ficus sundaica), one in Java (C. bergi) and one in Sulawesi (C. sumatranae).
The distribution of Conidarnes does not overlap with distribution of the two other genera belonging to the same clade. Indeed, Anidarnes is restricted to America (Farache et al. 2013), and Pseudidarnes occurs in Papua New Guinea, Australia, and the Solomon Islands (Farache and Rasplus 2014). This pattern corresponds to the distribution of their host Ficus species: section Americana (host of Anidarnes) is Neotropical, whereas section Malvanthera (host of Pseudidarnes) mostly occurs in Australia and New Guinea. Conidarnes is strictly associated with Conosycea, a section of figs occurring from India to Solomon Islands, with two species reaching Madagascar (Berg 1989;Farache et al. 2013;Farache and Rasplus 2014). The section Conosycea probably originated in continental Eurasia and subsequently spread through the islands of Southeast Asia, reaching Australasia and Madagascar (Cruaud et al. 2012).
Another characteristic of Sycophaginae species belonging to the clade of large gall inducers is that they are rare and globally difficult to sample (Cruaud et al. 2011b). Conidarnes and Pseudidarnes species are among the rarest Sycophaginae (Cruaud et al. 2011b;Farache et al. 2013;Farache and Rasplus 2014). These characteristics plus the difficulty to find and sample ripening hemi-epiphytic stranglers (Conosycea) in the jungle explain why several species described here are only known from one or a few specimens. Sampling of Conidarnes is always extremely difficult and sporadic. To exemplify this point, we only sampled 6 males of C. sulcata despite collecting and opening about 5000 figs of F. altissima in southern China. Consequently, we only obtained sequences from a few of these species (three) and we therefore encourage extensive sampling of Conosycea figs to improve our knowledge of the genus.