Abstract
Holometabolan larvae are dominating components of modern terrestrial and freshwater ecosystems and have a significant ecological impact. Also in past ecosystems, various types of such larvae have been present, which is especially well known from ambers from all over the world. During the Cretaceous, holometabolan larvae with a very modern appearance co-occur with those of morphologies totally unknown in the ecosystems of today. One of these morphologies only known from ca. 100-million-year-old Kachin amber from Myanmar is represented by the so-called “beak larvae”, which possess an anteriorly projecting beak-like mouth cone, previously being described from two specimens. We describe here a third specimen as a new species, ?Partisaniferus edjarzembowskii sp. nov. This new species differs from the previously described beak larva species Partisaniferus atrickmuelleri in the shape of the trunk end as well as in lacking a differentiation of the tergites into distinct sclerites and in the absence of abdomen protrusions. We discuss possible aspects of the ontogeny of the beak larvae, including the possibility that the here described specimen and one of the previously known ones are different larval stages of ?P. edjarzembowskii sp. nov. Furthermore, we discuss possible relationships of beak larvae within Neuropteriformia.
References
- Álvarez-Parra, S., Pérez-de la Fuente, R., Peñalver, E., Barrón, E., Alcalá, L., Pérez-Cano, J., Martín-Closas, C., Trabelsi, K., Meléndez, N., López Del Valle, R., Lozano, R.P., Peris, D., Rodrigo, A., Sarto i Monteys, V., Bueno-Cebollada, C.A., Menor-Salván, C., Philippe, M., Sánchez-García, A., Peña-Kairath, C., Arillo, A., Espílez, E., Mampel, L. & Delclós, X. (2021) Dinosaur bonebed amber from an original swamp forest soil. eLife, 10, e72477. https://doi.org/10.7554/eLife.72477
- Aspöck, U. & Aspöck, H. (2007) Verbliebene Vielfalt vergangener Blüte. Zur Evolution, Phylogenie und Biodiversität der Neuropterida (Insecta: Endopterygota). Denisia, 20, Kataloge des Oberösterreichischen Landesmuseums (Neue Serie), 66, 451–516.
- Badano, D., Engel, M.S., Basso, A., Wang B. & Cerretti P. (2018) Diverse Cretaceous larvae reveal the evolutionary and behavioural history of antlions and lacewings. Nature Communications, 9, 3257. https://doi.org/10.1038/s41467-018-05484-y
- Badano, D., Fratini, M., Maugeri, L., Palermo, F., Pieroni, N., Cedola, A., Haug, J.T., Weiterschan, T., Velten, J., Mei, M., Di Giulio, A. & Cerretti, P. (2021) X-ray microtomography and phylogenomics provide insights into the morphology and evolution of an enigmatic Mesozoic insect larva. Systematic Entomology, 46, 672–684. https://doi.org/10.1111/syen.12482
- Baranov, V., Haug, C., Fowler, M., Kaulfuss, U., Müller, P. & Haug, J.T. (2022) Summary of the fossil record of megalopteran and megalopteran-like larvae, with a report of new specimens. Bulletin of Geosciences, 97, 89–108. https://doi.org/10.3140/bull.geosci.1840
- Baranov, V.A., Wang, Y., Gašparič, R., Wedmann, S. & Haug, J.T. (2020) Eco-morphological diversity of larvae of soldier flies and their closest relatives in deep time. PeerJ, 8, e10356. https://doi.org/10.7717/peerj.10356
- Batelka, J. & Engel, M.S. (2022) The ̒first fossil tumbling flower beetle’ larva is a symphytan (Hymenoptera). Acta Entomologica Musei Nationalis Pragae, 62, 57–59. https://doi.org/10.37520/aemnp.2022.005
- Batelka, J., Engel, M.S. & Prokop, J. (2021) The complete life cycle of a Cretaceous beetle parasitoid. Current Biology, 31, R101–R119. https://doi.org/10.1016/j.cub.2020.12.007
- Batelka, J., Prokop, J., Pohl, H., Bai, M., Zhang, W. & Beutel, R.G. (2019) Highly specialized Cretaceous beetle parasitoids (Ripiphoridae) identified with optimized visualization of microstructures. Systematic Entomology, 44, 396–407. https://doi.org/10.1111/syen.12331
- Beutel, R.G., Zhang, W.W., Pohl, H., Wappler, T. & Bai, M. (2016) A miniaturized beetle larva in Cretaceous Burmese amber: reinterpretation of a fossil “strepsipteran triungulin”. Insect Systematics & Evolution, 47, 83–91. https://doi.org/10.1163/1876312X-46052134
- Cruickshank, R.D. & Ko, K. (2003) Geology of an amber locality in the Hukawng Valley, northern Myanmar. Journal of Asian Earth Sciences, 21, 441–455. https://doi.org/10.1016/S1367-9120(02)00044-5
- Fischer, T.C. (2021) In search for the unlikely: Leaf-mining caterpillars (Gracillariidae, Lepidoptera) from Upper Cretaceous and Eocene ambers. Zitteliana, 95, 135–145. https://doi.org/10.3897/zitteliana.95.63317
- Gauweiler, J., Haug, C., Müller, P. & Haug, J.T. (2022) Lepidopteran caterpillars in the Cretaceous: were they a good food source for early birds? Palaeodiversity, 15, 45–59. https://doi.org/10.18476/pale.v15.a3
- Gepp, J. (1984) Erforschungsstand der Neuropteren-Larven der Erde (mit einem Schlüssel zur Larvaldiagnose der Familien, einer Ü̈bersicht von 340 beschreibenen Larven und 600 Literaturzitaten). In: Gepp, J., Aspöck, H. & Hölzel, H. (Eds), Progress in worldʼs neuropterology. Proceedings of the 1st International Symposium on Neuropterology, 22–26 September 1980, Graz, Austria. Privately printed, Graz, pp. 183–239.
- Grimaldi, D. & Engel, M.S. (2005) Evolution of the insects. Cambridge University Press, Cambridge, 755 pp.
- Grimaldi, D.A., Engel, M.S. & Nascimbene, P.C. (2002) Fossiliferous Cretaceous amber from Myanmar (Burma): its rediscovery, biotic diversity, and paleontological significance. American Museum Novitates, 3361, 1–71. https://doi.org/10.1206/0003-0082(2002)361<0001:FCAFMB>2.0.CO;2
- Grimaldi, D., Kathirithamby, J. & Schawaroch, V. (2005) Strepsiptera and triungula in Cretaceous amber. Insect Systematics & Evolution, 36, 1–20. https://doi.org/10.1163/187631205788912787
- Gustafson, G.T., Michat, M.C. & Balke, M. (2020) Burmese amber reveals a new stem lineage of whirligig beetle (Coleoptera: Gyrinidae) based on the larval stage. Zoological Journal of the Linnean Society, 189, 1232–1248. https://doi.org/10.1093/zoolinnean/zlz161
- Haug, C., Herrera-Flórez, A. F., Müller, P. & Haug, J. T. (2019a) Cretaceous chimera—an unusual 100-million-year old neuropteran larva from the “experimental phase” of insect evolution. Palaeodiversity, 12, 1–11. https://doi.org/10.18476/pale.v12.a1
- Haug, C., Haug, G.T., Zippel, A., van der Wal, S. & Haug, J.T. (2021e) The earliest record of fossil solid-wood-borer larvae—immature beetles in 99 million-year-old Myanmar amber. Palaeoentomology, 4 (4), 390–404. https://doi.org/10.11646/palaeoentomology.4.4.14
- Haug, G.T., Baranov, V., Wizen, G., Pazinato, P.G., Müller, P., Haug, C. & Haug, J.T. (2021a) The morphological diversity of long-necked lacewing larvae (Neuroptera: Myrmeleontiformia). Bulletin of Geosciences, 96, 431–457. https://doi.org/10.3140/bull.geosci.1807
- Haug, J.T. (2020a) Metamorphosis in crustaceans. In: Anger, K., Harzsch, S. & Thiel, M. (Eds), Developmental biology and larval ecology. Vol. 7. The natural history of the Crustacea. Oxford University Press, Oxford, pp. 254–283. https://doi.org/10.1093/oso/9780190648954.003.0009
- Haug, J.T. (2020b) Why the term “larva” is ambiguous, or what makes a larva? Acta Zoologica, 101, 167–188. https://doi.org/10.1111/azo.12283
- Haug, G.T., Haug, C. & Haug J.T. (2021b) The morphological diversity of spoon-winged lacewing larvae and the first possible fossils from 99 million-year-old Kachin amber, Myanmar. Palaeodiversity, 14, 133–152. https://doi.org/10.18476/pale.v14.a6
- Haug, G.T., Haug, C., Pazinato, P.G., Braig, F., Perrichot, V., Gröhn, C., Müller, P. & Haug, J.T. (2020a) The decline of silky lacewings and morphological diversity of long-nosed antlion larvae through time. Palaeontologia Electronica, 23, a39. https://doi.org/10.26879/1029
- Haug, G.T., Haug, C., van der Wal, S., Müller, P. & Haug, J.T. (2022a) Split-footed lacewings declined over time: indications from the morphological diversity of their antlion-like larvae. Paläontologische Zeitschrift, 96, 29–50. https://doi.org/10.1007/s12542-021-00550-1
- Haug, J.T., Baranov, V., Müller, P. & Haug, C. (2021c) New extreme morphologies as exemplified by 100 million-year-old lacewing larvae. Scientific Reports, 11, 20432. https://doi.org/10.1038/s41598-021-99480-w
- Haug, J.T., Baranov, V., Schädel, M., Müller, P., Gröhn, P. & Haug, C. (2020b) Challenges for understanding lacewings: how to deal with the incomplete data from extant and fossil larvae of Nevrorthidae? (Neuroptera). Fragmenta Entomologica, 52, 137–167. https://doi.org/10.13133/2284-4880/472
- Haug, J.T., Engel, M.S., Mendes dos Santos, P., Haug, G.T., Müller, P. & Haug, C. (early view) Declining morphological diversity in snakefly larvae during last 100 million years. Paläontologische Zeitschrift. https://doi.org/10.1007/s12542-022-00609-7
- Haug, J.T. & Haug, C. (2021) A 100 million-year-old armoured caterpillar supports the early diversification of moths and butterflies. Gondwana Research, 93, 101–105. https://doi.org/10.1016/j.gr.2021.01.009
- Haug, J.T., Haug, G.T., Zippel, A., van der Wal, S., Müller, P., Gröhn, C., Wunderlich, J., Hoffeins, C., Hoffeins, H.-W. & Haug, C. (2021d) Changes in the morphological diversity of larvae of lance lacewings, mantis lacewings and their closer relatives over 100 million years. Insects, 12, 860. https://doi.org/10.3390/insects12100860
- Haug, J.T., Müller, P. & Haug, C. (2018) The ride of the parasite: a 100-million-year old mantis lacewing larva captured while mounting its spider host. Zoological Letters, 4, 31. https://doi.org/10.1186/s40851-018-0116-9
- Haug, J.T., Müller, P. & Haug, C. (2019b) A 100-million-year old predator: a fossil neuropteran larva with unusually elongated mouthparts. Zoological Letters, 5, 29. https://doi.org/10.1186/s40851-019-0144-0
- Haug, J.T., Müller, P. & Haug, C. (2019c) A 100-million-year old slim insectan predator with massive venom-injecting stylets - a new type of neuropteran larva from Burmese amber. Bulletin of Geosciences, 94, 431–440. https://doi.org/10.3140/bull.geosci.1753
- Haug, J.T., Müller, P. & Haug, C. (2020d) A 100 million-year-old snake-fly larva with an unusually large antenna. Bulletin of Geosciences, 95, 167–177. https://doi.org/10.3140/bull.geosci.1757
- Haug, J.T., Pazinato, P.G., Haug, G.T. & Haug, C. (2020c) Yet another unusual new type of lacewing larva preserved in 100-million-year old amber from Myanmar. Rivista Italiana di Paleontologia e Stratigrafia, 126, 821–832. https://doi.org/10.13130/2039-4942/14439
- Haug, J.T., Schädel, M., Baranov, V. A. & Haug, C. (2020e) An unusual 100-million-year old holometabolan larva with a piercing mouth cone. PeerJ, 8, e8661. https://doi.org/10.7717/peerj.8661
- Haug, J.T., van der Wal, S., Gröhn, C., Hoffeins, C., Hoffeins, H.-W. & Haug, C. (2022b) Diversity and fossil record of larvae of three groups of lacewings with unusual ecology and functional morphology: Ithonidae, Coniopterygidae and Sisyridae. Palaeontologia Electronica, 25, a14. https://doi.org/10.26879/1212
- Haug, J.T., Zippel, A., Haug, G.T., Hoffeins, C., Hoffeins, H.-W., Hammel, J.U., Baranov, V. & Haug, C. (2021f) Texas beetle larvae (Brachypsectridae) – the last 100 million years reviewed. Palaeodiversity, 14, 161–183. https://doi.org/10.18476/pale.v14.a8
- Khramov, A.V., Bashkuev, A.S. & Lukashevich, E.D. (2020) The fossil record of long-proboscid nectarivorous insects. Entomological Review, 100, 881–968. https://doi.org/10.1134/S0013873820070015
- Kirejtshuk, A.G. & Azar, D. (2008) New taxa of beetles (Insecta, Coleoptera) from Lebanese amber with evolutionary and systematic comments. Alavesia, 2, 15–46.
- Labandeira, C.C., Yang, Q., Santiago-Blay, J.A., Hotton, C.L., Monteiro, A., Wang, Y.J., Goreva, Y., Shih, C.K., Siljeström, S., Rose, T.R., Dilcher, D.L. & Ren, D. (2016) The evolutionary convergence of mid-Mesozoic lacewings and Cenozoic butterflies. Proceedings of the Royal Society B: Biological Sciences, 283, 20152893. https://doi.org/10.1098/rspb.2015.2893
- Liu, H., Luo, C., Jarzembowski, E.A. & Xiao, C. (2022) Acanthochrysa langae gen. et sp. nov., a new lacewing larva (Neuroptera: Chrysopoidea) from mid-Cretaceous Kachin amber. Cretaceous Research, 133, 105146. https://doi.org/10.1016/j.cretres.2022.105146
- Liu, Q., Lu, X., Zhang, Q., Chen, J., Zheng, X., Zhang, W., Liu, X. & Wang, B. (2018a) High niche diversity in Mesozoic pollinating lacewings. Nature Communications, 9, 3793. https://doi.org/10.1038/s41467-018-06120-5
- Liu, X., Shi, G., Xia, F., Lu, X., Wang, B. & Engel, M.S. (2018b) Liverwort mimesis in a Cretaceous lacewing larva. Current Biology, 28, 1475–1481. https://doi.org/10.1016/j.cub.2018.03.060
- Liu, X., Zhang, W., Winterton, S.L., Breitkreuz, L.C. & Engel, M.S. (2016) Early morphological specialization for insect-spider associations in Mesozoic lacewings. Current Biology, 26, 1590–1594. https://doi.org/10.1016/j.cub.2016.04.039
- Liu, Y., Hakim, M. & Huang, D. (2020) First stratiomyomorphan larvae in the mid-Cretaceous amber from Myanmar (Diptera: Brachycera). Cretaceous Research, 106, 104265. https://doi.org/10.1016/j.cretres.2019.104265
- MacKay, M.R. (1970) Lepidoptera in Cretaceous amber. Science, 167, 379–380. https://doi.org/10.1126/science.167.3917.379
- Pérez-de la Fuente, R., Delclòs, X., Peñalver, E. & Engel, M.S. (2016) A defensive behavior and plant-insect interaction in Early Cretaceous amber–the case of the immature lacewing Hallucinochrysa diogenesi. Arthropod Structure and Development, 45, 133–139. https://doi.org/10.1016/j.asd.2015.08.002
- Pérez-de la Fuente, R., Delclòs, X., Peñalver, E., Speranza, M., Wierzchos, J., Ascaso, C. & Engel, M.S. (2012) Early evolution and ecology of camouflage in insects. Proceedings of the National Academy of Sciences (USA), 109, 21414–21419. https://doi.org/10.1073/pnas.1213775110
- Pérez-de la Fuente, R., Engel, M.S., Azar, D. & Peñalver, E. (2019) The hatching mechanism of 130-million-year-old insects: an association of neonates, egg shells and egg bursters in Lebanese amber. Palaeontology, 62, 547–559. https://doi.org/10.1111/pala.12414
- Pérez-de la Fuente, R., Engel, M.S., Delclòs, X. & Peñalver, E. (2020) Straight-jawed lacewing larvae (Neuroptera) from Lower Cretaceous Spanish amber, with an account on the known amber diversity of neuropterid immatures. Cretaceous Research, 106, 104200. https://doi.org/10.1016/j.cretres.2019.104200
- Pérez-de la Fuente, R., Peñalver, E., Azar, D. & Engel, M.S. (2018) A soil-carrying lacewing larva in Early Cretaceous Lebanese amber. Scientific Reports, 8, 16663. https://doi.org/10.1038/s41598-018-34870-1
- Perrichot, V. & Engel, M.S. (2007) Early Cretaceous snakefly larvae in amber from Lebanon, Myanmar, and France (Raphidioptera). American Museum Novitates, 3598, 1–11. https://doi.org/10.1206/0003-0082(2007)3598[1:ECSLIA]2.0.CO;2
- Pohl, H., Batelka, J., Prokop, J., Müller, P., Yavorskaya, M.I. & Beutel, R.G. (2018) A needle in a haystack: Mesozoic origin of parasitism in Strepsiptera revealed by first definite Cretaceous primary larva (Insecta). PeerJ, 6, e5943. https://doi.org/10.7717/peerj.5943
- Shi, G., Grimaldi, D.A., Harlow, G.E., Wang, J., Wang, J., Yang, M., Lei, W., Li, Q. & Li, X. (2012) Age constraint on Burmese amber based on U-Pb dating of zircons. Cretaceous Research, 37, 155–163. https://doi.org/10.1016/j.cretres.2012.03.014
- Ślipinśki, S.A. (1991) A monograph of the world Cerylonidae (Coleoptera; Cucujoidea). Part 1: introduction and higher classification. Annali del Museo Civico di Storia Naturale Giacomo Doria, 88, 1–273.
- Ślipinśki, A. & Lawrence, J.F. (2010) 10.29. Cerylonidae Billberg, 1820. In: Kükenthal, W., Leschen, R.A.B., Beutel, R.G. & Lawrence, J.F. (Eds), Morphology and systematics (Elateroidea, Bostrichiformia, Cucujiformia partim). Vol. 2. De Gruyter, Berlin, pp. 10–29. https://doi.org/10.1515/9783110911213.422
- Tillyard, R.J. (1918) Studies in Australian Neuroptera. No. 7. The life-history of Psychopsis elegans (Gueìrin). Proceedings of the Linnean Society of New South Wales, 43, 787–818.
- Tillyard, R.J. (1922) The life-history of the Australian moth-lacewing, Ithone fusca, Newman (Order Neuroptera Planipennia). Bulletin of Entomological Research, 13, 205–223. https://doi.org/10.1017/S000748530002811X
- Wang, B., Xia, F., Engel, M.S., Perrichot, V., Shi, G., Zhang, H., Chen, J., Jarzembowski, E.A., Wappler, T. & Rust, J. (2016) Debris-carrying camouflage among diverse lineages of Cretaceous insects. Science Advances, 2, e1501918. https://doi.org/10.1126/sciadv.1501918
- Wichard, W. (2017). Family Nevrorthidae (Insecta, Neuroptera) in mid-Cretaceous Burmese amber. Palaeodiversity, 10, 1–5. https://doi.org/10.18476/pale.v10.a1
- Xia, F., Yang, G., Zhang, Q., Shi, G. & Wang, B. (2015) Amber: life through time and space. Science Press, Beijing, viii + 197 pp.
- Yu, T.T., Kelly, R., Mu, L., Ross, A., Kennedy, J., Broly, P., Xia, F.Y., Zhang, H.C., Wang, B. & Dilcher, D. (2019) An ammonite trapped in Burmese amber. Proceedings of the National Academy of Sciences, 116, 11345–11350. https://doi.org/10.1073/pnas.1821292116
- Zhao, X., Zhao, X., Jarzembowski, E., Tian, Y. & Chen, L. (2020) The first record of brachypsectrid larva from mid-Cretaceous Burmese amber (Coleoptera: Polyphaga). Cretaceous Research, 113, 104493. https://doi.org/10.1016/j.cretres.2020.104493
- Zippel, A., Haug, C., Hoffeins, C., Hoffeins, H.-W. & Haug, J.T. (2022a) Expanding the record of larvae of false flower beetles with prominent terminal ends. Rivista Italiana di Paleontologia e Stratigrafia, 128, 81–104. https://doi.org/10.54103/2039-4942/17084
- Zippel, A., Haug, C., Müller, P. & Haug, J.T. (2022b) First fossil tumbling flower beetle-type larva from 99 million-year-old amber. Paläontologische Zeitschrift, 96, 219–229. https://doi.org/10.1007/s12542-022-00608-8
- Zippel, A., Kiesmüller, C., Haug, G.T., Müller, P., Weiterschan, T., Haug, C., Hörnig, M.K. & Haug, J.T. (2021) Long-headed predators in Cretaceous amber—fossil findings of an unusual type of lacewing larva. Palaeoentomology, 4 (5), 475–498. https://doi.org/10.11646/palaeoentomology.4.5.14