A New Fossil of Necrotauliidae (Insecta: Trichoptera) from the Jiulongshan Formation of China and Its Taxonomic Significance

Background Acisarcuatus variradius gen. et sp. nov., an extinct new species representing a new genus, is described from the Middle Jurassic Jiulongshan Formation in Daohugou Village, Inner Mongolia, China. Methodology/Principal Findings In this paper, we revised the diagnosis of Necrotauliidae Handlirsch, 1906. One new genus and species of Necrotauliidae is described. An analysis based on the fossil morphological characters clarified the taxonomic status of the new taxa. Conclusions/Significance New fossil evidence supports the viewpoint that the family Necrotauliidae belongs to the Integripalpia.


Introduction
The Amphiesmenoptera, comprising two distinctive insect orders: the Trichoptera and the Lepidoptera [1]. Trichoptera, or caddisflies, are holometabolous insects. Their bodies and wings are covered by bushy hairs, and the adults resemble moths in appearance. They are among the largest group of aquatic insects [1,2] and one of the most diverse groups of insects overall with more than 14,000 extant species and more than 680 fossil species [3]. Trichoptera include three living suborders: Annulipalpia, Integripalpia, and Spicipalpia [4], but the monophyly of Spicipalpia is disputable [2,5]. Species of the Permian suborder Protomeropina Sukatcheva (1980) [6] are sometimes placed in Trichoptera [7,8] and sometimes are considered representatives of the Amphiesmenoptera stem group or more distant lineages [9,10].
Here, we describe a new and unique male adult fossil specimen collected from the Daohugou beds. The beds consist of 100-150 m thick succession of grey-white or locally reddish, thinly bedded claystones, shales, siltstones and sandy mudstones with intercalated ash-fall tuffs and ignimbrites. It was radiometrically dated by 40 K/ 40 Ar at 164-165 Ma [26], which accorded with the Callovian-Oxfordian boundary interval of the latest Middle Jurassic, using the latest standard international time scale [27]. Although there has been controversial to the precise age and stratigraphic position [28,29]. The well-preserved fossils of insects and other animals also prove that the Daohugou fauna assemblages may correlate with the Middle Jurassic Yan-Liao biota [30]. This new fossil specimen is significant because of its well-preserved head, maxillary palps, fore-and hind wings, abdomen, and male genitalia. Most previously described representatives of the family were based only on fragmentary remnants and/or isolated wings [23,[31][32][33]. Thus, this new fossil is an important supplement to Necrotauliidae records and provides new evidence for studying their origin and evolution. The complete preservation of the new specimen enables us to determine the phylogenetic status of Necrotauliidae.

Material
The part and counterpart of the fossil specimen (CNU-TRI-NN2013001pc) are deposited in the Key Lab of Insect Evolution & Environmental Changes, College of Life Sciences, Capital Normal University, Beijing, China. No specific permits were required for the described field studies.

Nomenclatural Acts
The electronic version of this document does not represent a published work according to the International Code of Zoological Nomenclature (ICZN), and hence the nomenclatural acts contained in the electronic version are not available under that Code from the electronic edition. Therefore, a separate edition of this document was produced to ensure that numerous identical and durable copies were simultaneously obtainable (from the publication date noted on the first page of this article) to provide a public and permanent scientific record in accordance with Article 8.1 of the Code.
This published work and the nomenclatural acts it contains have been registered in Zoobank, the online registration system for the ICZN. The Zoobank LSIDs (Life Science Identifiers) can be resolved and the associated information viewed through any standard web browser by appending the LSID to the prefix ''http://zoobank.org''. The ISID for this publication is: urn:lsid:zoobank.org: pub:64E83F92-0277-4F41-BC5B-9732B6691611. The electronic edition of this work was published in a journal with an ISSN, and has been archived and is available from the following digital repositories: PubMed Central and LOCKSS.

Methods
The fossil specimen was examined using a Leica MZ12.5 dissecting microscope (Wetzlar, Germany) and illustrated with the aid of a drawing tube attachment. When observing the details, the specimen was put under pure alcohol. Line drawings were made by Photoshop 9.0 graphic software (Adobe Systems, San Jose, CA, USA). Photographs were taken with a Nikon Digital Camera DXM 1200C (Tokyo, Japan).
Body length was measured from the apex of the head to the apex of the abdomen. The wing length was measured from the base to the apex of the wing. The length of antennae was measured from the base to the apex.

Remark
According to the new fossil, we added the characters on head, antennae, maxillary palps and tibial spur formula. On hind wing, M with only 3 branches on the previously reported specimens, but our specimen has M four-branched, thus we revised this character.

Diagnosis
Warts present on head. Forewing with 5 forks (I-V); Sc forked, Sc 2 straight and long, extending into pterostigma region; anal veins form a typical anal loop; discoidal cell short and closed, median cell and thyridial cell very long and open. Male genitalia harpagones regularly curving mesad, narrowing at apex; median phallic apparatus seems to be spicular and arcuate.

Etymology
The generic name is a combination of the Latin word acis (tip) and arcuatus (arc, curve), describing the peculiar curving of R1; gender masculine.

Distribution
China.

Description
Head with saponaceous triangle, compound eye at head sides, oval. Anterior setal warts and posterior setal warts present surrounding compound eye, irregularly oval. Antennae filiform but not well-preserved, scape slightly thicker than pedicel and flagellum, pedicel cylindrical, flagellum slender, length of segments equal to their diameter. Maxillary palps five-segmented; segment I swollen, segment II longest, segment III subequal to IV, segment V indistinct.
Thorax: Pronotum with one pair of setal warts, symmetrically drop-shaped. Mesothorax with triquetrous scutellum. Legs well-preserved. Foretibial spur   invisible, mesotibia with two apical spurs; metatibia with two preapical spurs and one or two apical spurs; tibial spur formula: 0: 2: 3 or 4. Fore tarsus five-segmented, slender, segment I longest, II-IV subequal in length; mesotarsus five-segmented, all tarsal segments with terminal spinules. Tarsal claw visible. Forewings elongated elliptic; Rs 4 terminating slightly below apex of forewing. Forewing with forks I-V; Sc forked, Sc 2 slightly bend terminally and ending into C at about 2/3 the length of forewing, Sc 1 terminating into C at about 2/3 length of Sc; R 1 unforked distally, straight in basal part and curved in pterostigma area; Rs forked at mid-length of the forewing; Dc short and closed by r 3 -r 4 ; F1 forks before than F2; Rs 1 slight bent towards R 1 at terminus; M originating from base of R; M forking before Rs forks; F3 and F4 longer than their stems; F3 forks later than Abdomen: In dorsal view, eight sternites visible and male genitalia prominent, bearing pair of two-segmented gonopods; coxopodite broad at base and shorter than harpago. Harpagones regularly curving mesad, narrowing at apex. Coxopodites and harpagos with dense hairs around margin. Middle preanal appendage and periphallus visible, median phallic apparatus seems to be spicular and arcuate. External structural details of male genitalia indistinct in fossil.

Remark
In our specimen, only one apical spur is visible, but the presence of another apical spur cannot be excluded (i.e. absent due to incomplete preservation).

Discussion
Kristensen provided a summary of 21 apomorphies supporting the monophyletic group of Amphiesmenoptera, with both Trichoptera and Lepidoptera certain features (e.g. forewing the terminal of the anal vein fusion) [37]. Furthermore, the monophylies of Trichoptera and Lepidoptera are also generally accepted [9]. Insect fossil caddisflies are generally preserved incompletely or indistinctly, and often only forewing is visible on the fossil [32,33]. Many paleontologists considered Necrotauliidae to be a representative of the amphiesmenopteran stem-group, and proximal to the common ancestor of trichopterans and lepidopterans that survived after the Triassic [1, 11-14, 17-21, 38]. This viewpoint is mainly based on the characteristics of forewing.
Our specimen possesses very clear male genitalia with harpagones (coxopodite broad at base and shorter than harpago), middle preanal appendage, spicular and arcuate median phallic apparatus. The harpagones is a synapomorphy of Trichoptera [5,24]. Beside that, maxillary palps of the new fossil specimen correspond to the apomorphy of Integripalpia [39,40]: maxillary palps upturned, with segment I swollen, densely hairs or scales invisible, segment II longest, segment III subequal to IV. The character that crossvein m absent is also similar to suborder Integripalpia [40]. On the basis of these characters, we believe Necrotauliidae is belongs to Integripalpia (Trichoptera).
Meanwhile A. variradius gen. et sp. nov. has some plesiomorphies of Integripalpia: Sc forked; forewing with five forks; crossveins very rare on both forewing and hind wing; only two crossveins, r and m-cu 1 present. These characters also can be found in the extinct suborder Protomeropina [6,[41][42][43]. It is interesting to speculate that necrotauliids are representatives of the Integripalpia stem-group rather than the amphiesmenopteran.