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Hidden diversity of small predators: new thorny lacewings from mid-Cretaceous amber from northern Myanmar (Neuroptera: Rhachiberothidae: Paraberothinae)

Published online by Cambridge University Press:  07 April 2020

Hiroshi Nakamine Open the ORCID record for Hiroshi Nakamine [Opens in a new window] ,
Shûhei Yamamoto Open the ORCID record for Shûhei Yamamoto [Opens in a new window]  and
Yui Takahashi Open the ORCID record for Yui Takahashi [Opens in a new window]
Hiroshi Nakamine*
Affiliation:
Minoh Park Insect Museum, Minoh Park 1–18, Minoh City, Osaka562-0002, Japan
Shûhei Yamamoto
Affiliation:
Integrative Research Center, Field Museum of Natural History, 1400 S Lake Shore Drive, Chicago, IL60605-2496, USA
Yui Takahashi
Affiliation:
Muroto Global Geopark Center, Murotomisaki-cho 1810-2, Muroto City, Kochi781-7101, Japan
*
Author for correspondence: Hiroshi Nakamine, Email: nakamine.konchu@osaka.email.ne.jp
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Abstract

Thorny lacewings (Rhachiberothidae) are currently distributed only within Africa, whereas they are prevalent in the fossil record of various Cretaceous ambers across the Northern Hemisphere, with a handful of the fossil records from some Eocene European ambers. Four rhachiberothid species in four extinct genera are known from the mid-Cretaceous amber of northern Myanmar. Here, we report further examples of the remarkable palaeodiversity of this group from the same amber deposit, adding the four new fossil genera and seven new species: Acanthoberotha cuspis gen. et sp. nov., Astioberotha falcipes gen. et sp. nov., Stygioberotha siculifera gen. et sp. nov., Uranoberotha chariessa gen. et sp. nov., Creagroparaberotha cuneata sp. nov., Micromantispa galeata sp. nov. and M. spicata sp. nov. Based on a series of well-preserved specimens, we discuss the fine details of the raptorial forelegs and genital segments, which may be important for elucidating the phylogenetic relationships among genera. Our findings reveal an unexpectedly diverse assemblage of thorny lacewings in the Cretaceous System, highlighting the morphologically diverse rhachiberothids in Burmese amber. The discovery of seven additional rhachiberothid species in Myanmar amber suggests the potential for much higher diversity and abundance of the Cretaceous rhachiberothids than previously documented. Furthermore, morphological variation in the raptorial forelegs was found to be extremely diverse among the Burmese amber paraberothines, especially in terms of the size, number and shape of spines (or spine-like setae) on the inner edges of protibia, and the morphological structure of the probasitarsus.

Keywords

MantispoideaRhachiberothidaeParaberothinaeMyanmarCenomanian
Type
Original Article
Information
Geological Magazine , Volume 157 , Issue 7 , July 2020 , pp. 1149 - 1175
Copyright
© Cambridge University Press 2020

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References

Aspöck, U and Aspöck, H (1997) Studies on new and poorly-known Rhachiberothidae (Insecta: Neuroptera) from sub-Saharan Africa. Annalen des Naturhistorischen Museums in Wien 99B, 1–20.Google Scholar
Aspöck, U and Aspöck, H (2008) Phylogenetic relevance of the genital sclerites of Neuropterida (Insecta: Holometabola). Systematic Entomology 33, 97–127, doi: 10.1111/j.1365-3113.2007.00396.x.CrossRefGoogle Scholar
Aspöck, U, Haring, E and Aspöck, H (2012) The phylogeny of the Neuropterida: long lasting and current controversies and challenges (Insecta: Endopterygota). Arthropod Systematics & Phylogeny 70, 119–29.Google Scholar
Aspöck, U and Mansell, M (1994) A revision of the family Rhachiberothidae Tjeder, 1959, stat. n. (Neuroptera). Systematic Entomology 19, 181–206, doi: 10.1111/j.1365-3113.1994.tb00587.x.CrossRefGoogle Scholar
Aspöck, U, Plant, JD and Nemeschkal, HL (2001) Cladistic analysis of Neuroptera and their systematic position within Neuropterida (Insecta: Holometabola: Neuropterida: Neuroptera). Systematic Entomology 26, 73–86, doi: 10.1046/j.1365-3113.2001.00136.x.CrossRefGoogle Scholar
Aspöck, U and Randolf, S (2014) Beaded lacewings – a pictorial identification key to the genera, their biogeographics and a phylogentic analysis (Insecta: Neuroptera: Berothidae). Deutsche Entomologische Zeitschrift 61, 155–72, doi: 10.3897/dez.61.8850.CrossRefGoogle Scholar
Azar, D, Gèze, R and Acra, F (2010) Lebanese amber. In Biodiversity of Fossils in Amber from the Major World Deposits (ed. Penney, D), pp. 271–98. Manchester, UK: Siri Scientific Press.Google Scholar
Bakkes, DK, Sole, CL and Mansell, MW (2017) Revision of Afrotropical silky lacewings (Neuroptera: Psychopsidae). Zootaxa 4362, 152–212, doi: 10.11646/zootaxa.4362.2.1.CrossRefGoogle Scholar
Brannoch, SK, Wieland, F, Rivera, J, Klass, K-D, Béthoux, O and Svenson, GJ (2017) Manual of praying mantis morphology, nomenclature, and practices (Insecta, Mantodea). ZooKeys 696, 1–100, doi: 10.3897/zookeys.696.12542.CrossRefGoogle Scholar
Breitkreuz, LCV, Winterton, SL and Engel, MS (2017) Wing tracheation in Chrysopidae and Other Neuropterida (Insecta): a resolution of the confusion about vein fusion. American Museum Novitates 3890, 1–44, doi.org/10.1206/3890.1.CrossRefGoogle Scholar
Brunke, AJ, Chatzimanolis, S, Metscher, BD, Wolf-Schwenninger, K and Solodovnikov, A (2017) Dispersal of thermophilic beetles across the intercontinental Arctic forest belt during the early Eocene. Scientific Reports 7, 12972, doi: 10.1038/s41598-017-13207-4.CrossRefGoogle ScholarPubMed
Cai, W and Tomokuni, M (2003) Camptibia obscura, gen. and sp. nov. (Heteroptera: Reduviidae: Harpactorinae) from China. European Journal of Entomology 100, 181–5, doi: 10.14411/eje.2003.028.CrossRefGoogle Scholar
Crighton, WR and Carrio, V (2007) Photography of amber inclusions in the collections of National Museums Scotland. Scottish Journal of Geology 43, 89–96, doi: 10.1144/sjg43020089.CrossRefGoogle Scholar
Cruickshank, RD and Ko, K (2003) Geology of an amber locality in the Hukawng Valley, northern Myanmar. Journal of Asian Earth Sciences 21, 441–55, doi: 10.1016/S1367-9120(02)00044-5.CrossRefGoogle Scholar
Engel, MS (2004) Thorny lacewings (Neuroptera: Rhachiberothidae) in Cretaceous amber from Myanmar. Journal of Systematic Palaeontology 2, 137–40, doi: 10.1017/S1477201904001208.CrossRefGoogle Scholar
Engel, MS and Grimaldi, DA (2008) Diverse Neuropterida in Cretaceous amber, with particular reference to the paleofauna of Myanmar (Insecta). Nova Supplementa Entomologica 20, 1–86.Google Scholar
Engel, MS, Winterton, SL and Breitkreuz, LCV (2018) Phylogeny and evolution of Neuropterida: where have wings of lace taken us? Annual Review of Entomology 63, 531–51, doi: 10.1146/annurev-ento-020117-043127.CrossRefGoogle ScholarPubMed
Grimaldi, DA (2000) A diverse fauna of Neuropterodea in amber from the Cretaceous of New Jersey. In Studies on Fossil in Amber, with Particular Reference to the Cretaceous of New Jersey (ed. Grimaldi, DA), pp. 259–303. Leiden: Backhuys Publishers.Google Scholar
Grimaldi, DA, Engel, MS and Nascimbene, PC (2002) Fossiliferous Cretaceous amber from Myanmar (Burma): its rediscovery, biotic diversity, and paleontological significance. American Museum Novitates 3361, 1–71, doi: 10.1206/0003-0082(2002)361<0001:FCAFMB>2.0.CO;2.2.0.CO;2>CrossRefGoogle Scholar
Grimaldi, DA and Ross, AJ (2017) Extraordinary Lagerstätten in amber, with particular reference to the Cretaceous of Burma. In Terrestrial Conservation Lagerstätten: Windows into the Evolution of Life on Land (eds Fraser, NC and Sues, H-D), pp. 287–342. Edinburgh: Dunedin Academic Press.Google Scholar
Jarzembowski, EA (1999) British amber: a little-known resource. In Proceedings of the World Congress on Amber Inclusions, Vitoria-Gasteiz, 1998. Estudios del Museo de Ciencias Naturales de Alava 14, 133–40.Google Scholar
Jepson, JE (2015) A review of the current state of knowledge of fossil Mantispidae (Insecta: Neuroptera) Zootaxa 3964, 419–32, doi: 10.11646/zootaxa.3964.4.2.CrossRefGoogle ScholarPubMed
Jepson, JE, Heads, SW, Makarkin, VN and Ren, D (2013) New fossil Mantidflies (Insecta: Neuroptera: Mantispidae) from the Mesozoic of North-Eastern China. Palaeontology 56, 603–13, doi: 10.1111/pala.12005.CrossRefGoogle Scholar
Jepson, JE, Khramov, AV and Ohl, M (2018) New Mesomantispinae (Insecta: Neuroptera: Mantispidae) from the Jurassic of Karatau, Kazakhstan. Zootaxa 4402, 563–74, doi: 10.11646/zootaxa.4402.3.9.CrossRefGoogle ScholarPubMed
Khramov, AV (2013) New mantidflies (Neuroptera: Mantispidae) from Upper Jurassic of Kazakhstan and Mongolia. Insect Systematics & Evolution 44, 221–30.CrossRefGoogle Scholar
Lambkin, KJ (1986) A revision of the Australian Mantispidae (Insecta: Neuroptera) with a contribution to the classification of the family. I. General and Drepanicinae. Australian Journal of Zoology Supplementary Series 116, 1–142.Google Scholar
Leach, WE (1815) Entomology. In Edinburgh Encyclopaedia (ed. Brewster, D), Vol. 9, pp. 57–172. Edinburgh: William Blackwood.Google Scholar
Linnaeus, C (1758) Systema Naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis, vol. 1, 10th edn. Holmiae: Laurentii Salvii, iii + 824 pp.Google Scholar
Liu, X, Aspöck, H, Winterton, S, Zhang, W and Aspöck, U (2017) Phylogeny of pleasing lacewings (Neuroptera: Dilaridae) with a revised generic classification and description of a new subfamily. Systematic Entomology 42, 448–71, doi: 10.1111/syen.12225.CrossRefGoogle Scholar
Liu, X, Winterton, S, Wu, C, Piper, R and Ohl, M (2015) A new genus of mantidflies discovered in the Oriental region, with a higher-level phylogeny of Mantispidae (Neuroptera) using DNA sequences and morphology. Systematic Entomology 40, 183–206, doi: 10.1111/syen.12096.CrossRefGoogle Scholar
Makarkin, VN (2015a) A new genus of the mantispid-like Paraberothinae (Neuroptera: Berothidae) from Burmese amber, with special consideration of its probasitarsus spine-like setation. Zootaxa 4007, 327–42, doi: 10.11646/zootaxa.4007.3.2.CrossRefGoogle ScholarPubMed
Makarkin, VN (2015b) An important new fossil genus of Berothinae (Neuroptera: Berothidae) from Bultic amber. Zootaxa 3946, 401–15, doi: 10.11646/zootaxa.3946.3.7.CrossRefGoogle ScholarPubMed
Makarkin, VN (2015c) A remarkable new genus of Mantispidae (Insecta, Neuroptera) from Cretaceous amber of Myanmar and its implications on raptorial foreleg evolution in Mantispidae: a comment. Cretaceous Research 52, 423–4, doi: 10.1016/j.cretres.2014.06.012.CrossRefGoogle Scholar
Makarkin, VN and Kupryjanowicz, J (2010) A new mantispid-like species of Rhachiberothinae from Baltic amber (Neuroptera, Berothidae), with a critical review of the fossil record of the subfamily. Acta Geologica Sinica 84, 655–64, doi: 10.1111/j.1755-6724.2010.00238.x.CrossRefGoogle Scholar
Mao, Y, Liang, K, Su, Y, Li, J, Rao, X, Zhang, H, Xia, F, Fu, Y, Cai, C and Huang, D (2018) Various amberground marine animals on Burmese amber with discussions on its age. Palaeoentomology 1, 91–103, doi: 10.11646/palaeoentomology.1.1.11.CrossRefGoogle Scholar
Mc Kellar, RC and Engel, MS (2009) A new thorny lacewing (Neuroptera: Rhachiberothidae) from Canadian Cretaceous amber. Journal of the Kansas Entomological Society 82, 114–21, doi: 10.2317/JKES811.10.1.CrossRefGoogle Scholar
Nakamine, H and Yamamoto, S (2018) A new genus and species of thorny lacewing from Upper Cretaceous Kuji amber, northeastern Japan (Neuroptera, Rhachiberothidae). ZooKeys 802, 109–20, doi: 10.3897/zookeys.802.28754.CrossRefGoogle Scholar
Nel, A, Perrichot, V, Azar, D and Néraudeau, D (2005a) New Rhachiberothidae (Insecta: Neuroptera) in Early Cretaceous and Early Eocene ambers from France and Lebanon. Neues Jahrbuch für Geologie und Paläontologie Abhandlungen 235, 51–85.Google Scholar
Nel, A, Perrichot, V, Azar, D and Néraudeau, D (2005b) A replacement name for the neuropteran genus Eorhachiberotha Nel et al., 2005 (Neuroptera: Rhachiberothidae). Bulletin de la Société Entomologique de France 110, 128.Google Scholar
Ohl, M (2005) Towards a global inventory of Mantispidae - the state-of-theart in mantispid taxonomy. In Proceedings of the Ninth International Symposium on Neuropterology, Ferrara, Italy, 20–23 June 2005 (eds Pantaleoni, RA, Letardi, A and Corazza, C), pp. 79–86. Ferrera, Italy: Annali del Museo Civico di Storia Naturale di Ferrara, 8.Google Scholar
Oswald, JD (1993) Revision and cladistic analysis of the world genera of the family Hemerobiidae (Insecta: Neuroptera). Journal of New York Entomological Society 101, 143–299.Google Scholar
Oswald, JD (2019) Neuropterida Species of the World. Version 6.0. Available at http://lacewing.tamu.edu/SpeciesCatalog/Main (accessed 11 February 2020).Google Scholar
Panfilov, DV (1980) New representatives of lacewings (Neuroptera) from the Jurassic of Karatau. In Fossil Insects of the Mesozoic (eds Dolin, VG, Panfilov, DV, Ponomarenko, AG and Pritykina, LN), pp. 82–111. Kiev: Naukova Dumka.Google Scholar
Penney, D and Green, DI (2010) Introduction, preparation, study & conservation of amber inclusions. In Biodiversity of Fossils in Amber from the Major World Deposits (ed. Penney, D), pp. 5–21. Manchester: Siri Scientific Press.Google Scholar
Pérez-de la Fuente, R and Peñalver, E (2019) A mantidfly in Cretaceous Spanish amber provides insights into the evolution of integumentary specialisations on the raptorial foreleg. Scientific Reports 9, 1–16, doi: 10.1038/s41598-019-49398-1.CrossRefGoogle ScholarPubMed
Petrulevičius, JF, Azar, D and Nel, A (2010) A new thorny lacewing (Insecta: Neuroptera: Rhachiberothidae) from the Early Cretaceous amber of Lebanon. Acta Geologica Sinica 84, 828–33, doi: 10.1111/j.1755-6724.2010.00242.x.CrossRefGoogle Scholar
Poinar, G Jr (2019) Burmese amber: evidence of Gondwanan origin and Cretaceous dispersion. Historical Biology 31, 1304–9, doi: 10.1080/08912963.2018.1446531.Google Scholar
Poinar, G Jr and Beckley, R (2011) Doratomantispa burmanica n. gen., n. sp. (Neuroptera: Mantispidae), a new genus of mantidflies in Burmese amber. Historical Biology 23, 169–76, doi: 10.1080/08912963.2010.505024.CrossRefGoogle Scholar
Riek, EF (1955) Fossil insects from the Triassic beds at Mt. Crosby, Queensland. Australian Journal of Zoology 3, 654–91, doi: 10.1071/ZO9550654.CrossRefGoogle Scholar
Ross, AJ (2019) Burmese (Myanmar) amber checklist and bibliography 2018. Palaeoentomology 2, 22–84, doi: 10.11646/palaeoentomology.2.1.5.CrossRefGoogle Scholar
Schlüter, T (1978) Zur Systematik und Paläkologie harzkonservierter Arthropoda einer Taphozönose aus dem Cenomanium von NW-Frankreich. Berliner Geowissenschaftliche Abhandlungen A9, 1–150.Google Scholar
Shi, G, Grimaldi, DA, Harlow, GE, Wang, J, Wang, J, Yang, M, Lei, W, Li, Q and Li, X (2012) Age constraint on Burmese amber based on U-Pb dating of zircons. Cretaceous Research 37, 155–63, doi: 10.1016/j.cretres.2012.03.014.CrossRefGoogle Scholar
Shi, C, Ohl, M, Wunderrich, J and Ren, D (2015) A remarkable new genus of Mantispidae (Insecta, Neuroptera) from Cretaceous amber of Myanmar and its implications on raptorial foreleg evolution in Mantispidae. Cretaceous Research 52, 416–22, doi: 10.1016/j.cretres.2014.04.003.CrossRefGoogle Scholar
Song, N, Li, X-X, Zhai, Q, Bozdoğan, H and Yin, XM (2019) The mitochondrial genomes of Neuropteridan insects and implications for the phylogeny of Neuroptera. Genes 10, 108, doi: 10.3390/genes10020108.CrossRefGoogle ScholarPubMed
Tjeder, B (1959) Neuroptera-Planipennia: The lace-wings of southern Africa. 2. Family Berothidae. In South African Animal Life (eds Hanström, B, Brinck, P and Rudebeck, G), Vol. 6, pp. 256–314. Stockholm, Sweden: Swedish Natural Science Research Council.Google Scholar
Wedmann, S and Makarkin, VN (2007) A new genus of Mantispidae (Insecta: Neuroptera) from the Eocene of Germany, with a review of the fossil record and palaeobiogeography of the family. Zoological Journal of the Linnean Society 149, 701–16, doi: 10.1111/j.1096-3642.2007.00273.x.CrossRefGoogle Scholar
Westerweel, J, Roperch, P, Licht, A, Dupont-Nivet, G, Win, Z, Poblete, F, Ruffet, G, Swe, HH, Thi, MK and Aung, DW (2019) Burma Terrane part of the Trans-Tethyan arc during collision with India according to palaeomagnetic data. Nature Geoscience 12, 863–8, doi: 10.1038/s41561-019-0443-2.CrossRefGoogle ScholarPubMed
Whalley, PES (1980) Neuroptera (Insecta) in amber from the Lower Cretaceous of Lebanon. Bulletin of the British Museum of Natural History (Geology) 33, 157–64.Google Scholar
Whalley, PES (1983) Fera venatrix gen. and sp. n. (Neuroptera: Mantispidae) from amber in Britain. Neuroptera International 2, 229–33.Google Scholar
Wichard, W (2016) Overview and descriptions of Nevrorthidae in Baltic amber (Insecta, Neuroptera). Palaeodiversity 9, 95–111, doi: 10.18476/pale.v9.a7.CrossRefGoogle Scholar
Wieland, F (2013) The phylogenetic system of Mantodea (Insecta: Dictyoptera). Species, Phylogeny and Evolution 3, 3–222, doi: 10.17875/gup2013-711.Google Scholar
Winterton, SL, Hardy, NB and Wiegmann, BM (2010) On wings of lace: phylogeny and Bayesian divergence time estimates of Neuropterida (Insecta) based on morphological and molecular data. Systematic Entomology 35, 349–78, doi: 10.1111/j.1365-3113.2010.00521.x.CrossRefGoogle Scholar
Winterton, SL, Lemmon, A, Gillung, JP, Garzon, IJ, Badano, D, Bakkes, DK, Breitkreuz, LCV, Engel, MS, Lemmon, EM, Liu, XY, Machado, RJP, Skevington, JH and Oswald, JD (2018) Evolution of lacewings and allied orders using anchored phylogenomics (Neuroptera, Megaloptera, Raphidioptera). Systematic Entomology 43, 330–54, doi: 10.1111/syen.12278.CrossRefGoogle Scholar
Yu, T, Kelly, R, Mu, L, Ross, A, Kennedy, J, Broly, P, Xia, F, Zhang, H, Wang, B and Dilcher, D (2019) An ammonite trapped in Burmese amber. Proceedings of the National Academy of Sciences 116, 11345–50, doi: 10.1073/pnas.1821292116.CrossRefGoogle ScholarPubMed
Zhang, J, Gordon, ERL, Forthman, M, Hwang, WS, Walden, K, Swanson, DR, Johnson, KP, Meier, R and Weirauch, C (2016) Evolution of the assassinʼs arms: insights from a phylogeny of combined transcriptomic and ribosomal DNA data (Heteroptera: Reduvioidea). Scientific Reports 6, 22177, doi: 10.1038/srep22177.CrossRefGoogle Scholar
Zhao, P, Pham, M, Truong, X and Cai, W (2014) Flexitibia, a new genus of Harpactorinae (Hemiptera: Heteroptera: Reduviidae), with a discussion on the functional morphology of forelegs of the related genera. Zootaxa 3795, 564–70, doi: 10.11646/zootaxa.3795.5.5.CrossRefGoogle Scholar
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