Giant Jurassic dragon lacewing larvae with lacustrine palaeoecology represent the oldest fossil record of larval neuropterans

Abstract

Neuropterans seem to be less specious among holometabolans, while they are in fact the relicts of a diverse group from the Mesozoic era. Their early radiation resulted in great family level morphological heterogeneity of extant neuropterans, especially of their larvae. The earliest previously reported fossil larvae of this group were from the Early Cretaceous, where they already showed high taxonomic diversity and an extremely wide range of variations in morphotypes. In this work, the earliest record of the larva of the neuropteran Palaeoneurorthus baii gen. et sp. nov. from the Middle Jurassic Daohugou Beds of China is described. The larvae, which have large and elongated bodies, straight stylets with curved apices, an extremely elongated cervix and an extended anterior lobe of pronotum, are placed in Nevrorthidae. The elongated cervix is probably a specialized adaptation for hunting small organisms. The palaeoenvironment of these larvae indicates that larvae of Nevrorthidae have exhibited stable aquatic ecology since the Middle Jurassic, and underwent a possible shift from lakes to more lotic yet constricted modern mountain rivulet habitats over time.

1. Introduction

Neuroptera is a relatively small group of Holometabolans with 16 major extant lineages and about 11 fossil families [1,2]. The adults are commonly known as lacewings, mantis lacewings (Mantispidae) and owlflies (Ascalaphinae/Ascalaphidae) and have lacey, colourful membranous wings and delicate bodies [3]. The larvae of neuropterans are peculiar in appearance and possess a pair of mandibulo-maxillary stylets in front of their heads [2]. Because of their adaptive radiation in hunting behaviours, the larvae have a broad morphological spectrum. Most modern lineages are represented by distinct larval morphotypes, and larvae may look quite different even within some closely related families and subfamilies [4,5].

The immature stage is the key phase for neuropterans. Immature individuals usually spend a significant part of their lives in dramatically different lifestyles and have a greater ecological impact than adult forms [6]. Records of immature neuropterans are rather incomplete compared to the abundant fossils of adult lacewings. Although the neuropterans had reached a peak of diversity in the Middle Jurassic to the Early Cretaceous [7], there are no documented larva predating the Early Cretaceous, except for an undescribed and unfigured Middle Jurassic ‘nevrorthid-like’ larva [2].

The oldest larvae previously reported are chrysopoid from Barremian (ca. 130 Ma, the Early Cretaceous) Lebanese amber [8,9]. Other Mesozoic fossil records include Nevrorthidae, Berothidae, Chrysopidae, Hemerobiidae, Nymphidae, Psychopsidae, Mesochrysopidae, Mantispidae, Nemopteridae, Myrmeleontidae and stem-group myrmeleontiformians (e.g. [10–17]), as well as questionable Osmylidae and Dilaridae [18]. Most notably, the Kachin amber (the early Cenomanian: approximately 99 Ma) has a rich assemblage of larvae fossils with diverse taxa and morphological disparity [19], with some ‘experimental forms’ that adopted extreme morphologies not found in extant taxa [20,21]. From an overall point of view, the evolution of larvae is far from being resolved [22]. This is probably because the fossils hitherto reported did not possess enough antiquity to implicate the earlier diversification of this group. Here we formally report new larvae of Nevrorthidae from the Daohugou Konservat-Lagerstätte of China, extending the knowledge of immature neuropterans from the Cretaceous back to the Middle Jurassic and providing new insights into the ecology of the primitive neuropterans.

2. Material and methods

The holotype YLSNHM01098, deposited in the Yingliang Stone Natural History Museum in Fujian, China, and paratype specimen NIGP201165, deposited in the Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences (NIGPAS), were excavated from the Daohugou Beds, Jiulongshan Formation (also referred to as the Haifanggou Formation by some authors) of Ningcheng County, Inner Mongolia, China (locality given in [23]). These fossil strata have been recognized as a lacustrine fossil Lagerstätte associated with volcanic–sedimentary tectonics [24], in which numerous freshwater and terrestrial crustaceans, insects, vertebrates and plants are exceptionally preserved [25].

The Daohugou strata consist of tuffaceous conglomerate, tuffaceous siltstone and tuff, non-conformably on Archean gneiss and are overlain by the volcanic breccia of the Tiaojishan Formation in angular unconformity ([26], stratigraphic column in [27]). The age of the Daohugou fossil beds has long been debated. Radiometric dating of the overlying Tiaojishan Formation yields different data between 152–170 Ma ([24], 255). A small number of researchers [28] have questioned whether the stratigraphic sequence had been overturned, but this is not widely accepted, and the minimum age is generally considered to be between 166 and 159 Ma (Bathonian–Callovian), close to the Middle–Upper Jurassic boundary [29].

The described fossils herein were preserved as compressions in tuffaceous siltstone together with several freshwater conchostracans and fragments of other insects. YLSNHM01098 is only accessible dorsally, the counterparts of head and cervix are missing, and its abdominal segments are poorly preserved. NIGP201165 is preserved with its counterpart. Preliminary observations and preparations were made using an Olympus SZX61 stereomicroscope. Photographs of YLSNHM01098 were taken with a Nikon SMZ25 stereomicroscope with built-in software, both dry and in alcohol. NIGP201165 was documented with a Nikon Z7II camera and a Zeiss V16 stereomicroscope system with ZEN software, then rendered with Helicon Focus software using the depth map method. The images were optimized in Adobe Photoshop 2021 software, including the correction of the white balance, brightness and contrast. Plates were prepared using Adobe Illustrator 2021.

The morphological terminology used for the head morphology herein follows MacLeod [30] and Beutel et al. [31], while body measurements and terminology in this article generally follow Haug et al. [32].

3. Results

(a) . Systematic palaeontology

Insecta Linnaeus, 1758

Neuroptera Linnaeus, 1758

Osmyloidea Panfilov, 1980

Nevrorthidae Nakahara, 1915

Palaeoneurorthus gen. nov.

LSID (Life Science Identifier): urn:lsid:zoobank.org:act:356204A8-8E97-49C7-952F-EBB8EDDB3000

Diagnosis: as for the species.

Etymology: the generic name consists of Latin ‘palaeo-’ which indicates the antiquity of this taxon, and ‘Neurorthus’, the type genus of Nevrorthidae.

Type species: Palaeoneurorthus baii sp. nov.

Type locality: Daohugou Village, Ningcheng County, NE China.

Horizon and age: Jiulongshan Formation, upper Middle Jurassic.

Repository: Holotype: Yingliang Stone Nature History Museum, China. Paratype: Nanjing Institute of Geology and Palaeontology, China Academy of Sciences.

Palaeoneurorthus baii sp. nov.

LSID: urn:lsid:zoobank.org:act:399B7B6F-A53C-4CF6-8861-4C19FBF590E6

Diagnosis: i) large body size, ii) rostrum not developed, iii) cervix extremely elongated, twice the length of the head capsule, narrower than the head capsule and prothorax.

Etymology: the specific name is dedicated to Bai Bingyang, who provided the holotype for research.

Type: Holotype: YLSNHM01098, a nearly complete larva. Paratype: NIGP201165

(NIGP201165a, b, part and counterpart, respectively), a nearly complete larva. The two specimens are considered final instar larvae due to their greatly elongated abdomen compared to the size of the head capsule.

Description of holotype YLSNHM01098

A final instar larva with large body size, 41.2 mm long, measured from head to abdominal apex without stylets; divided into head, cervix and trunk; body greatly elongated, tapers anteriorly and posteriorly, with the greatest width at abdominal elements I∼III. (figure 1a)

Figure 1.

Holotype of Palaeoneurorthus baii gen. et sp. nov., larva (YLSNHM01098) from the Daohugou Beds, Ningcheng County, China. (a) Photograph of the complete body (dry), (b) drawing of the complete body, (c) photograph of head and anterior half of cervix (in alcohol), (d) colour marked version of head and cervix. a1–a9, abdominal element 1–9, cs, coronal suture, cv, cervix, fe, femur, fs, frontal suture, md, mandible, ms, mesothorax, mt, metathorax, mxst, maxillary stylet, P2, setae on the posterior parietal region (tentatively homologized setae, see reference [31]), pl, palpus labialis, pt, prothorax, S3, ventrolateral setae on the rounded temples, tar, tarsus, te, trunk end, ti, tibia, tr, trochanter. Scale bars = 10 mm (a, a1), 2 mm (b, b1). 178 × 164 mm (300 × 300 DPI).

Head: prognathous, suboval, L/W ratio = 1.88, lateral margins sub-parallel to each other and slightly widened anteriorly, with the greatest width near the base of stylets; basal part of the head capsule strongly narrowed to a neck connected to the cervix, width at base is 0.34 mm. Stylets 3.30 mm long, elongated and slender, slightly broadened basally and tapering towards apex into a sharp point; straight proximally and only curved inward apically, without any dentation. Labial palps with at least two segments, inserted between the paired mouthparts. Rostrum undeveloped; stemmata not visible. Antennomeres not preserved. Frontal sutures and coronal suture intersect on the anterior 1/3 of the head capsule, frontal sutures V-shaped posteriorly, anterior part not observable, lateral parietal ridge present, long and thin setae on the posterior parietal region (?P₂), and anterolaterally on the rounded temples (S₃), (figure 1b).

Cervix: extremely slender and elongated, 5.27 mm long at midline, about 0.5 mm wide, parallel-sided but slightly widened on both ends, apparently narrower than head and pronotum; well-sclerotized, with a median suture; bearing equally spaced long setae laterally.

Thorax: prothorax 1.98 mm long, pronotum sclerotized, covering the anterior half of prothorax, the median part of anterior margin strongly forward-extending to 1/4 of the cervix, mesothorax and metathorax elongated, mesothorax 5.91 mm long, metathorax 4.53 mm long.

Legs: Pro-, meso- and meta-thoracic legs similar in shape. Front legs: coxa nearly invisible, trochanter 1.05 mm long, broadened in the middle part, femur also somewhat broadened or inflated, tibia slender and straight. Middle legs: coxa robust, trochanter inflated, shorter than protrochanter, femur also inflated, slightly curved distally, tibia slender, tarsus partly preserved, nearly straight. Hind legs: almost as same as middle legs.

Abdomen: greatly elongated, almost worm-like, bearing sparse long setae, elements I to V similar in shape, but element I is more compressed, elements VI to VIIII are more elongated than previous five segments, the maximum length abdomen is from III to V, abdomen tapering from IV both anteriorly and posteriorly, abdominal apex poorly preserved, bearing setae from element IV.

Description of paratype NIGP201165

Description: possible final instar larva, very large body size, 43.9 mm long, measured from head to abdominal apex without stylets; the body is clearly divided into head, cervix, thorax and abdomen; body greatly elongated, tapers anteriorly and posteriorly, with the greatest width at the first abdominal element (figure 2a,b).

Figure 2.

Paratype of Palaeoneurorthus baii gen. et sp. nov., larva (NIGP201165) from the Daohugou Beds, Ningcheng County, China. (a) Photograph of the complete body (dry), (b) drawing of the complete body, (c) photograph of counterpart (dry). a1–a9, abdominal element 1–9, cv, cervix, cx, coxa, fe, femur, hc, head capsule, mt, metathorax, ms, mesothorax, pt, prothorax, st, stylet, tar, tarsus, te, trunk end, ti, tibia, tr, trochanter. Scale bar equals 10 mm. 178 × 172 mm (300 × 300 DPI).

Head: prognathous, suboval, length 2.60 mm, L/W ratio = 1.85, slightly narrowed posteriorly, posterior part of the head capsule strongly narrowed connecting to the cervix. Stylets formed by mandibles and maxillae, slightly broadened basally. Labial palps at least with four segments, inserted between the paired mouthparts, 1st segment short, 2nd and 3rd segments slender, about four times long as wide, 2nd segment is nearly three times the length of the 1st segment. Prementum not visible, more probably obscured by the upper exoskeleton than absent. Rostrum undeveloped, only forming a simple rounded lobe. Antennae filiform, with five preserved antennomeres, inserted next to the mouthparts, extending towards the side front; each article identical in shape, twice long as wide. Frontal sutures and coronal suture intersect on the front 1/3 of the head capsule, forming a V-shaped frontal region. Lateral parietal ridge present (figures 3 and 4).

Figure 3.

Head of paratype NIGP201165. (a) photography of head, in alcohol, (b) drawing of head, (c), photograph of head of the counterpart, in alcohol, (d) drawing of counterpart head. ant, antennae, cv, cervix, cs, coronal suture, fs, frontal suture, lpr, lateral parietal ridge, md: mandible, mxst, maxillary stylets, ne, neck region, P2, setae on the posterior parietal region (see reference [31]), pl, palpus labialis, rg, Rollengelenk, S3, ventrolateral setae on the rounded temples. Note that (c) and (d) are the counterpart of compression fossil, not the ventral view of larval head. Scale bar equals 1 mm. 267 × 122 mm (300 × 300 DPI).

Figure 4.

Ecological reconstruction of Palaeoneurorthus baii gen. et sp. nov. (by Bai Bingyang). The colours are artistic only. 177 × 132 mm (300 × 300 DPI).

Cervix: extremely slender and elongated, 5.52 mm long at midline, 0.71 mm anteriorly, about 0.68 mm wide on average, narrower than head and pronotum; well-sclerotized and bearing setae laterally; with a median suture; possible trace of a pair of Rollengelenk (roller joints) near the anterior lateral of cervix.

Thorax: prothorax 2.16 mm long. Pronotum sclerotized, trapezoid shaped, lateral margins tapering anteriorly, the anterior lobe extending forward to a triangular protrusion. Mesothorax and metathorax slightly elongated; mesothorax 6.03 mm long; metathorax 4.83 mm long.

Legs: bearing sparse long setae. Front legs: coxa invisible; trochanter broadened in the middle part; femur also somewhat broadened, 1.46 mm long; tibia slender and straight, longer than femur, tarsus about 2/3 length of the tibia; two tarsal claws about 1/5 the length of tibia, curved inward, with one triangular tooth on the inner side. Middle legs: coxa robust; trochanter inflated; shorter than precoxa; femur also inflated, slightly curved distally; tibia slender; tarsus partly preserved, nearly straight. Hind legs: almost the same as middle legs, but with broader femur; tarsal claws paired, same as those of the front leg.

Abdomen: greatly elongated, almost worm-like, tapering from element I or II. Thin setae are visible near the abdominal apex.

4. Discussion

(a) . Taxonomy

This fossil larva is assigned to the order Neuroptera based on i) the sucking jaws formed by the mandibles and maxillae [30,33] and ii) the presence of a cervix (sclerotized region between head and pronotum) [33]. The coexistence of the larvae with abundant freshwater conchostracans and other aquatic larvae (in the same strata) and little evidence of transportation, suggest that Palaeoneurorthus baii gen. et sp. nov. is in an autochthonous state from a shallow lacustrine environment [34]. This coincides with the larval ecology of Osmyloidea, which is the only lineage with fully aquatic immatures among known neuropterans [2,35].

Within Osmyloidea, the distally curved mouthparts of larvae are distinct from the straight, needle-like mouthparts of the Sisyridae and Osmylidae, and closely resemble those of extant Nevrorthidae. This feature is likely an autapomorphy of Nevrorthidae in the superfamily [31].

The specimens conforms to the following morphological diagnosis of Nevrorthidae: i) proximally straight stylets with a curved tip and no dentation [31,36,37]; ii) a narrowed neck region of the head capsule [31]; iii) the presence of an elongated and sclerotized cervix [32]; and iv) an elongated and almost worm-like abdomen [32], distinguishing them from the conical and slender abdomen of aphid lions, as well as the compressed and broad trunk of antlions [4,38]. The ‘Rollengelenk’ (roller joint connecting the head capsule and cervix) that is considered to be a potential autapomorphy of the family [31,36] is probably preserved in the paratype.

Therefore, the specimens were assigned to Nevrorthidae, and differed from all other known larvae of this family due to their remarkably large hiatus, undeveloped rostrum, extremely slender and elongated cervix twice the length of the head capsule, and the presence of a triangular protrusion on the anterior lobe of the pronotum. Though lacking a robust fossil record in the early Mesozoic, the nevrorthids are considered a basal group of Neuroptera [39–42]. Molecular cladistic estimations point to a Late Triassic to Jurassic origin of the stem-group nevrorthids [43–46], thus further supporting this taxonomic placement.

(b) . Palaeoecology

The larvae of modern Nevrorthids are aquatic or semi-aquatic, inhabiting the bottom of clear mountain streams or moist litter in cool temperate climates [31,39,47,48]. They are ambush predators that feed on small soft-bodied organisms using the pair of piercing–sucking stylets, which is similar to those of other neuropteran families [32]. The Jurassic fossil larvae inhabited a palaeoenvironment comprising lakes, swamps and rivulets in a hilly area, with a humid, warm to medium temperate climate with seasonal changes according to a study on the Daohugou flora [49]. Considering the taphonomy of Daohugou fossil beds, the fossil larvae were aquatic and possibly lived at the bottom of shallow lakes. In addition to indicating the overall stability in the aquatic larval habitats of Nevrorthidae since the Middle Jurassic, the presence of the larvae in a lacustrine deposit also revealed that they inhabited a more stable environment than their extant counterparts in fast-moving streams.

The body size of P. baii is a very impressive feature, being distinctively larger than all known extant and extinct Nevrorthidae larvae. P. baii, is also the largest fossil larval neuropteran reported to date, surpassing the large larvae in the mid-Cretaceous Kachin amber, including the one incomplete Psychopsidae head from which it was estimated to have a body length of 30 mm (specimen 52 in [50]), and Kuafupolydentes hui Luo et al., 2022 with long and robust legs and massive stylets [19]. Previous described Nevrorthidae larvae do not exceed 13 mm [32]; in contrast, P. baii have body lengths of over 40 mm. This may have resulted from the difference of habitat; extant Nevrorthidae have only been found in constricted places, thus limiting their body size. Moreover, the shallow lake deposit, which has yielded abundant fossils of potential prey, could have provided a wider range of food sources than a mountain stream environment.

The extremely elongated cervix resembled those of the extant larvae of Crocinae (Neuroptera: Nemopteridae), is clearly a convergency considering the very distant relationship between the families. We assume that the cervix of Palaeoneurorthus had a comparable function, which was an adaptation for predation while concealing its large abdomen and maintaining distance between its delicate abdomen and the struggling prey [51].

5. Conclusion

The earliest and largest recorded neuropteran larval fossils from the Daohugou Biota (the Middle Jurassic) are described. Palaeoneuruorthus gen. nov. has a close affinity with the extant family Nevrorthidae. This taxon adds new data to the larval morphology of basal neuropterans and provides new insights into the palaeoecology of earlier neuropterans, suggesting the lacustrine larval ecology in this group in the Middle Jurassic.

Data accessibility

The micro-photographs of the specimens in this article have been uploaded to FigShare (https://doi.org/10.6084/m9.figshare.c.6422549) [52].

Authors' contributions

X.D.: writing—original draft, writing—review and editing; K.N.: project administration, writing—original draft; T.B.: funding acquisition, project administration, supervision, writing—original draft, writing—review and editing.

All authors gave final approval for publication and agreed to be held accountable for the work performed therein.

Conflict of interest declaration

We declare we have no competing interests.

Funding

This research was supported by research grants from the Sun Yat-sen University Hundred-Talent Programme (grant no. 77010-12220013), the National Natural Science Foundation of China (grant nos. 42293280, 42288201), the State Key Laboratory of Biogeology and Environmental Geology Open Fund (grant no. GBL22101), the Shenzhen Science and Technology Program (grant nos. 202206193000001, 20220815111354002), and the Strategic Priority Research Program of the Chinese Academy of Sciences (grant no. XDB26000000).