Two New Fossil Sawflies of Pamphiliidae (Hymenoptera: Symphyta) from the Mesozoic of Northeastern China †

Simple Summary Two new species and one new specimen of Scabolyda (Pamphiliidae) are described from the Mesozoic of northeastern China. Structures of antennae, genitalia, and legs, especially the hind tarsal claw, are preserved. The documentation of these new structures helps to link extant and fossil taxa of Pamphiliidae. Abstract Two new species of Pamphiliidae, Scabolyda latusa sp. nov. and Scabolyda tenuis sp. nov. are described and illustrated from the late Middle Jurassic Jiulongshan Formation and the Lower Cretaceous Yixian Formation of northeastern China, respectively. A new specimen of Scabolyda orientalis Wang, Rasnitsyn, Shih and Ren, 2014 with distinct male genitalia is documented for the first time. Based on the specimens with new and distinct structures of legs, antennae, and genitalia, the morphological characters of Scabolyda are supplemented: antenna with ca. 13–14 flagellomeres; fore leg with tibia without pre-apical spur; hind leg nearly 0.6 times as long as the body, hind tarsal claw without setae and its inner tooth not developed. In addition, the tarsal claw characteristics found in the new species may suggest Scabolyda has a closer relationship with Cephalciinae, rather than with Pamphiliinae.

Diagnosis. Large body size (nearly 20 mm in length). Body surface with obvious punctations, especially on head and thorax. Antenna with the first flagellomere nearly 4× as long as the second flagellomere; the ratio of length to width of the following flagellomere nearly two; forewing with vein 4-Rs present and short. Hind tarsal claw with inner tooth small, located submedial.
Description (Figures 2 and 3). Holotype. Female. Head very pale with black areas on part of postocellar area, frons, and gena; many obvious punctations surrounding the ocellus and around the postocellar area and gena. The whole antenna pale brown, except for the basal scape blackish. Thorax color pale with the lateral mesothorax and partial metathorax black; mesonotum and metanotum densely covered with punctations. Hind leg pale brown except for the coxa blackish. The whole abdomen and forewing pale brown ( Figure 2).
Head massive and flat, its width about 1.2× length; postocellar furrow and lateral furrow visible; middle fovea and lateral fovea indistinct; frons weakly raised. Eyes medium-sized and nearly half the length of head; temple obviously raised. Antenna ca. 2.3× Etymology. The specific name "latusa" (latus = wide) is a Latin word, referring to the broad antenna of this species.
Diagnosis. Large body size (nearly 20 mm in length). Body surface with obvious punctations, especially on head and thorax. Antenna with the first flagellomere nearly 4× as long as the second flagellomere; the ratio of length to width of the following flagellomere nearly two; forewing with vein 4-Rs present and short. Hind tarsal claw with inner tooth small, located submedial.
Description (Figures 2 and 3). Holotype. Female. Head very pale with black areas on part of postocellar area, frons, and gena; many obvious punctations surrounding the ocellus and around the postocellar area and gena. The whole antenna pale brown, except for the basal scape blackish. Thorax color pale with the lateral mesothorax and partial metathorax black; mesonotum and metanotum densely covered with punctations. Hind leg pale brown except for the coxa blackish. The whole abdomen and forewing pale brown ( Figure 2).
Head massive and flat, its width about 1.2× length; postocellar furrow and lateral furrow visible; middle fovea and lateral fovea indistinct; frons weakly raised. Eyes mediumsized and nearly half the length of head; temple obviously raised. Antenna ca. 2.3× as long as the width of head, and the left antenna 15-segmented; scape 3.9× as long as pedicel, and 0.9× as wide as apical pedicel, its length shorter than the first flagellomere; pedicel 0.2× as long, and almost as wide as the first flagellomere; the first flagellomere 4.9× as long as wide and ca. 3.9× the length of the second flagellomere; the second flagellomere 1.6× as long as wide and slightly shorter than the third flagellomere, each of the remaining flagellomeres not more than 2.3× as long as wide and gradually thinning toward the apex.
Thorax with pronotum 0.8× as wide as head; mesothorax wider than head, with notaulices, parapsidal suture, mesoprescutum, and mesoscutellum visible. Mesoprescutum about half of mesoscutum in width, and larger than mesoscutellum. Metathorax with metapostnotum and parapsis visible, cenchrus indistinct. Leg with hind leg visible, full of setae, and its length longer than abdomen; coxa large, inverted trapeziform, not reaching half of abdomen; trochanter and trochantellus visible. Femur markedly thick and with five spurs obviously present; middle part of femur thicker than basal part but not reaching twice. Tibia thin and nearly 1.3× as long as femur. Tarsus partly visible; claw with two teeth and the inner tooth small ( Figure 2E).
Abdomen with seven segments preserved. Ovipositor as preserved typical of Pamphilioidea: very short, with stylets (valvula 1 and valvula 2) widely separated basally and meeting only at the apex ( Figure 2D).
Forewing with pterostigma slender and sclerotized, and about 3.6× as long as wide. Sc bifid; Sc2 shorter than Sc1 and entering R before 1-Rs; R bent strongly near the middle part. 1-Rs approximately 0.5× as long as 1-M and nearly as long as 1r-rs, inclined toward wing apex; 1r-rs ca. 0.4× as long as 2r-rs. 2r-m parallel to 2r-rs, meeting Rs slightly distal to 2r-rs. 3r-m inclined toward wing apex and meeting 5-Rs nearly at 121 • ; Rs+M 1.3× as long as 1-M; 1-M meeting 1-Cu at an angle of 127 • ; M+Cu obviously bending and without stub around the corner. Cell 1 mcu ca. 1.3× as long as wide, with cu-a located distad the middle of cell. 2-M and Rs+M nearly equal in length; 3-Cu at least 2.8× as long as 1 m-cu; 2 m-cu curved near its middle. Cell 2a ca. 3.5× as long as wide. Hind wing with Sc present, reclined and longish. 1-Rs nearly as long as 1-M. Both 1A and 2A bent, and 2A more curved than 1A.
Paratype. Female. Head flat, full of punctations, and significantly raised on both sides. Mandibles well-developed and mostly occupying more than half width of the head, with a large submedial inner tooth on both sides ( Figure 3C,D). Eyes medium-sized, nearly half length of head. Lateral furrow vaguely visible.
Thorax with punctations. Mesothorax with mesoprescutum, mesoscutellum, and mesoscutellar appendage visible. Cenchrus slightly smaller than mesoscutellar appendage. Hind leg with coxa, trochanter and femur preserved, coxa inverted trapezoid and nearly reaching the posterior margin of the second tergite. Abdomen with eight segments, ovipositor short and incompletely preserved.
Forewing nearly reaching the seventh tergite. Pterostigma long and sclerotized. Sc developed and forked; Sc2 joining R proximal to 1-Rs and the distance between them about its own length. Radial vein obviously curved at the middle part.  Etymology. The Latin name "tenuis" meaning thin, referring to the long and slender flagellomere of this species.
Diagnosis. Body surface without punctations. Flagellomeres, except for the first flagellomere, slender and long, more than three times as long as wide. Forewing with Sc1 and Sc2 nearly equal in length; 2r-rs and 2r-m almost in a line, 4-Rs absent.
Description (Figure 4). Holotype. Sex unknown. Head, thorax and abdomen brown and without punctations. The basal scape color dark brown; the rest part of scape and the first flagellomere brown; the other flagellomeres light yellow. Veins of forewing and hind wing with color ocher and without any wrinkles (Figure 4). Etymology. The Latin name "tenuis" meaning thin, referring to the long and slender flagellomere of this species.
Diagnosis. Body surface without punctations. Flagellomeres, except for the first flagellomere, slender and long, more than three times as long as wide. Forewing with Sc1 and Sc2 nearly equal in length; 2r-rs and 2r-m almost in a line, 4-Rs absent.
Description (Figure 4). Holotype. Sex unknown. Head, thorax and abdomen brown and without punctations. The basal scape color dark brown; the rest part of scape and the first flagellomere brown; the other flagellomeres light yellow. Veins of forewing and hind wing with color ocher and without any wrinkles (Figure 4). Head massive and flat, nearly 1.6× as wide as long; postocellar furrow and lateral furrow visible. Eye medium-sized and its bottom part below the postocellar furrow. Antenna partly preserved, at least ten segments; scape 0.7× as long as the first flagellomere, nearly as wide as pedicel; pedicel trapezoidal. The first flagellomere lightly dilated, 4.5× as long as wide, and nearly as long as the sum of next three segments; the second flagellomere 3.6× as long as wide; other flagellomeres left (some preserved incompletely) ca. 3.5× as long as wide.
Thorax slightly wider than head; pronotum partly preserved; mesoscutum faintly visible, nearly inverted triangle. Mesoprescutum larger than mesoscutellum. The remaining part of the thorax not discernible. Abdomen with eight segments preserved; the first segment divided medially. Genitalia poorly preserved, thus sex unknown.
Forewing with pterostigma long and sclerotized, ca. 3.7× as long as wide. Sc forked and its main vein located nearly at the middle of costal area; Sc2 almost as long as Sc1, Head massive and flat, nearly 1.6× as wide as long; postocellar furrow and lateral furrow visible. Eye medium-sized and its bottom part below the postocellar furrow. Antenna partly preserved, at least ten segments; scape 0.7× as long as the first flagellomere, nearly as wide as pedicel; pedicel trapezoidal. The first flagellomere lightly dilated, 4.5× as long as wide, and nearly as long as the sum of next three segments; the second flagellomere 3.6× as long as wide; other flagellomeres left (some preserved incompletely) ca. 3.5× as long as wide.
Thorax slightly wider than head; pronotum partly preserved; mesoscutum faintly visible, nearly inverted triangle. Mesoprescutum larger than mesoscutellum. The remaining part of the thorax not discernible. Abdomen with eight segments preserved; the first segment divided medially. Genitalia poorly preserved, thus sex unknown.
Forewing with pterostigma long and sclerotized, ca. 3.7× as long as wide. Sc forked and its main vein located nearly at the middle of costal area; Sc2 almost as long as Sc1, and both of them entering vein R or C before the base of 1-Rs ( Figure 4D); 1-Rs inclined apically Remarks. The two new species are assigned to Pamphiliidae for the same reasons in the remarks for the new specimen of Scabolyda orientalis above. Both new species can be further attributed to the Scabolyda based on the combination of these morphological characters: antenna with the first flagellomere nearly three times as long as the second flagellomere; forewing with pterostigma slender, Sc developed and forked, Sc2 entering R proximal to 1-Rs, 1-Rs nearly half of 1-M in length, angle between 1-M and 1-Cu over 90 • , 2r-rs close to the apical pterostigma, and 3r-m inclined toward the wing apex.
With the descriptions of two new species, the Mesozoic pamphiliids are diversified and the relevant character structures are expanded, such as antennae, legs, and genitalia. In order to better distinguish the four species of Scabolyda, we selected the key characters and established the relevant key to the identification of these four species of Scabolyda.

Discussion
As one of the basal groups in Symphyta, Pamphiliidae have very few Mesozoic fossil record and until now, there are only three species [7,14]. Some minute but important characters used for the classification of extant taxa are difficult to be preserved in compression fossils, such as the arrangement of the inner tooth in the tarsal claw, tibial spines, and spurs, either membranous or completely sclerotized at the tips, etc. [9,10]. In this study, we documented two new fossil species with well-preserved antennae and legs, which provided clearly visible characters to address the issues of unknown minute characters. With the addition of these features, it will be helpful to classify and identify species of Pamphiliidae with more than just venational characters commonly used for fossils.
The newly documented characters of antennae and legs in Scabolyda are as follows: antenna with ca. 13-14 flagellomeres, fore leg with tibia lacking pre-apical spur, mid leg with tibia having at least three spurs, hind leg nearly 0.6 times as long as the body, hind tibia with five spurs, the inner tooth of hind tarsal claw not developed and the claw without setae. Herein, we suggest treating these antenna and leg characters as diagnostic characters for Scabolyda as well.
After comparisons, the antenna is different at the species level and the leg, especially the tarsal claw of hind leg, is different at the subfamily level. Antennal morphology is an important character to distinguish different taxa in Pamphilioidea. Compared with other families, the scape and the first flagellomere are normal, and the length ratio between the first flagellomere and the second flagellomere is relatively stable (nearly 2-3 times) in Pamphiliidae [18]. However, the antennae for species of Scabolyda have diversified forms: the flagellomere is relatively widest in S. latusa sp. nov.; the first flagellomere is shortest in S. incompleta; length-width ratio of flagellomere (except the first flagellomere) is ca. 2-2.5 times in the Middle Jurassic Daohugou groups ( Figure 5A,B) and 3-4 times in the Lower Cretaceous Yixian groups ( Figure 5C,D). The main length-width ratio of flagellomeres and comparison of lengths are shown in Table 1. In spite of the differences, the possibility cannot be excluded that some reported species might belong to the same species for the existence of sexual dimorphism which is common in Hymenoptera [19]. In addition, some documented specimens with genital organs poorly-preserved made the comparison and judgment even more difficult.
After comparisons, the antenna is different at the species level and the leg, especially the tarsal claw of hind leg, is different at the subfamily level. Antennal morphology is an important character to distinguish different taxa in Pamphilioidea. Compared with other families, the scape and the first flagellomere are normal, and the length ratio between the first flagellomere and the second flagellomere is relatively stable (nearly 2-3 times) in Pamphiliidae [18]. However, the antennae for species of Scabolyda have diversified forms: the flagellomere is relatively widest in S. latusa sp. nov.; the first flagellomere is shortest in S. incompleta; length-width ratio of flagellomere (except the first flagellomere) is ca. 2-2.5 times in the Middle Jurassic Daohugou groups ( Figure 5A,B) and 3-4 times in the Lower Cretaceous Yixian groups ( Figure 5C,D). The main length-width ratio of flagellomeres and comparison of lengths are shown in Table 1. In spite of the differences, the possibility cannot be excluded that some reported species might belong to the same species for the existence of sexual dimorphism which is common in Hymenoptera [19]. In addition, some documented specimens with genital organs poorly-preserved made the comparison and judgment even more difficult.   The claw, usually located at the apex of the leg, plays an important role in support and sensing [20][21][22]. Ermolenko [23] used to study the tarsal claw structure in representative Symphyta and the shape of claw was later widely used as a taxonomic character. The two extant subfamilies of Pamphiliidae have different types of tarsal claw. In Cephalciinae, the claw is generally long and slender, which has a minute and perpendicular inner tooth, located submedial ( Figure 6A). While in Pamphiliinae, the claw is bifurcate and the basal part obviously broadened. The inner tooth is pointing to the apex of the claw and longer than its basal width ( Figure 6B) [17]. For the extinct Scabolyda in Juralydinae, the type of claw is very similar to that of Cephalciinae. The whole claw is slightly bent on the inner side and has a small and perpendicular tooth in the species S. latusa sp. nov. Moreover, there is no such minute tooth in S. orientalis ( Figure 6C), which may be the more basal (ancestor) condition of the claw and similar to that of the genus Xyela (Family Xyelidae) [21]. Moreover, the lengths of the setae covering the claws in extant groups often reach at least the lengths of the setae on their apical tarsomeres, while the setae were not developed or possibly absent in the extinct Scabolyda, as shown in specimens. The lack of setae on the claw of Scabolyda suggests that these extinct sawflies might have held less tarsal sensing efficiency when compared with the extant sawflies. The claw, usually located at the apex of the leg, plays an important role in support and sensing [20][21][22]. Ermolenko [23] used to study the tarsal claw structure in representative Symphyta and the shape of claw was later widely used as a taxonomic character. The two extant subfamilies of Pamphiliidae have different types of tarsal claw. In Cephalciinae, the claw is generally long and slender, which has a minute and perpendicular inner tooth, located submedial ( Figure 6A). While in Pamphiliinae, the claw is bifurcate and the basal part obviously broadened. The inner tooth is pointing to the apex of the claw and longer than its basal width ( Figure 6B) [17]. For the extinct Scabolyda in Juralydinae, the type of claw is very similar to that of Cephalciinae. The whole claw is slightly bent on the inner side and has a small and perpendicular tooth in the species S. latusa sp. nov. Moreover, there is no such minute tooth in S. orientalis ( Figure 6C), which may be the more basal (ancestor) condition of the claw and similar to that of the genus Xyela (Family Xyelidae) [21]. Moreover, the lengths of the setae covering the claws in extant groups often reach at least the lengths of the setae on their apical tarsomeres, while the setae were not developed or possibly absent in the extinct Scabolyda, as shown in specimens. The lack of setae on the claw of Scabolyda suggests that these extinct sawflies might have held less tarsal sensing efficiency when compared with the extant sawflies.  The characters of the claw found in these newly reported specimens suggest that Scabolyda might have a closer relationship with Cephalciinae, rather than with Pamphiliinae. At present, the species of extant Cephalciinae live in habitats full of conifers [9]. Furthermore, we explore the possibility that the Pamphiliidae also lived on coniferous plants in the Mesozoic. According to previous research, gymnosperms were dominant and most types of conifers were present in the Jurassic, peaking in the Late Jurassic to the Early Cretaceous [24], which happened to be the age Scabolyda reported. Additionally, a variety of conifer fossils have also been reported in the Daohugou Biota and Yixian Biota [25][26][27]. Therefore, based on the potential habitats in the Jurassic and the similar structures between Cephalciinae and Scabolyda, we suggest that the Jurassic species of Scabolyda might have lived on conifers as well. Some of them might have further adapted to conifers and established strong bonds in later evolution.

Conclusions
Due to the limitation on the preservation of fossil material, the classification of the extinct Pamphiliidae has previously mainly been based on wing venation, such as vein Sc developed or not, the relative length of 1-Rs, the width of the pterostigma, etc. However, the extant taxa are often classified through more diverse aspects, such as the surface colors, the spurs, and spines in tibia, the number of teeth in the mandible, and so on. This information asymmetry makes it hard to compare fossil and extant taxa in some characteristics, leading to weakened inter-relationships between them.
Although the fossil record of Pamphiliidae is currently small, researchers have tried to add features other than wing venation to the diagnostic characters. Rasnitsyn [4] added the shape of head, the segmentation of antenna, the width of the femur and the hollow of the last sternite in the diagnoses of genera of Atocus and Tapholyda. Wang et al. [16] described the characteristics of Scabolyda regarding the first to third flagellomeres and the scutum in mesothorax. Obviously, these characters are far from sufficient. In this study, we added the characteristics of antennae and legs in Scabolyda: antenna with ca. 13-14 flagellomeres; fore leg with tibia without pre-apical spur; hind leg nearly 0.6 times as long as the body, hind tarsal claw without setae, and its inner tooth small or absent.
We observed some differences in antennae among different species of Scabolyda, which may be due to the sexual dimorphism. The structures of the tarsal claw are rarely preserved and, thus, have not been reported in Symphyta fossils before. The hind tarsal claw of Scabolyda lacks setae and has a small and perpendicular inner tooth or is absent, which is morphologically more similar to that of Cephalciinae.

Data Availability Statement:
No new data were created or analyzed in this study. Data sharing is not applicable to this article.