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Type: Article
Published: 2018-08-01
Page range: 161–176
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Synonymize Arma chinensis as Arma custos based on morphological, molecular and geographical data

Department of Entomology, Shanxi Agricultural University, Taigu, Shanxi, China
Department of Entomology, Shanxi Agricultural University, Taigu, Shanxi, China
Institute of Entomology, College of Life Sciences, Nankai University, 94 Weijin Road, Tianjin, 300071, China
Institute of Entomology, College of Life Sciences, Nankai University, 94 Weijin Road, Tianjin, 300071, China
Department of Entomology, Shanxi Agricultural University, Taigu, Shanxi, China
Heteroptera Pentatomidae Asopinae Arma new synonym morphology DNA barcoding

Abstract

Arma custos and A. chinensis have a very conspicuous difference in the shape of the pronotal humeral angle, but the genitalic morphological characters are ambiguous and difficult to recognize. The aim of this study was to analyze the taxonomic status of A. chinensis and A. custos based on morphological, molecular, and geographical evidence, and to determine whether DNA barcoding could be a useful additional tool for differentiating similar species. The results clearly demonstrate that A. custos and A. chinensis have not diverged into separate species. So, the following new synonym is proposed: Arma chinensis Fallou, 1881 = Arma custos (Fabricius, 1794) syn. nov.. The results also showed that DNA barcoding using the marker COI can resolve insect taxonomic problems.

References

  1. Ahmad, I. & Önder, F. (1990) Revision of the genus Arma Hahn (Hemiptera: Pentatomidae: Pentatominae: Asopini) with description of two new species from Turkey. Türkiye Entomologii Dergisi, 14 (1), 3–12.

    Buj, I., Šanda, R., Marčić, Z., Ćaleta, M. & Mrakovčić, M. (2014) Combining Morphology and Genetics in Resolving Taxonomy– A Systematic Revision of Spined Loaches (Genus Cobitis; Cypriniformes, Actinopterygii) in the Adriatic Watershed. PLoS ONE, 9 (6), e99833.
    https://doi.org/10.1371/journal.pone.0099833

    Chantarasuwan, B., Berg, C.C., Kjellberg, F., Rønsted, N., Garcia, M., Baider, C. & van Welzen, P.C. (2015) A new classification of Ficus subsection Urostigma (Moraceae) based on four nuclear DNA markers (ITS, ETS, G3pdh, and ncpGS), morphology and leaf anatomy. PLoS ONE, 10 (6), e0128289.
    https://doi.org/10.1371/journal.pone.0128289

    Chen, F.Y. (1987) Hemiptera (Pentatomidae). In: Guo, Z.Z. (Eds.), The agricultural and forestry insect fauna of Guizhou. Vol. 1. Guizhou People’s Publishing House, Guiyang, pp.113–216, pls. IV–XIV. [in Chinese]

    Chow, S., Konishi, K., Mekuchi, M., Tamaki, Y. & Nohara, K. (2016) DNA barcoding and morphological analyses revealed validity of Diadema clarki Ikeda, 1939 (Echinodermata, Echinoidea, Diadematidae). ZooKeys, 585, 1–16.
    https://doi.org/10.3897/zookeys.585.8161

    Collins, R.A. & Cruickshank, R.H. (2014) Known knowns, known unknowns, unknown unknowns and unknown knowns in DNA barcoding: a comment on Dowton et al. Systematic biology, 63 (6), 1005–1009.
    https://doi.org/10.1093/sysbio/syu060

    Coulianos, C.C. (2005) Annotated checklist and distribution of the true bugs (Hemiptera- Heteroptera) of Estonia. Proceedings of the Estonian Academy of Sciences, Biology, Ecology, 54 (2), 136–165.

    Derzhansky, V.V., Kerzhner, I.M. & Danilovich, L.P. (2002) Holotypes and lectotypes of Palaearctic Pentatomoidea in the collection of the Zoological Institute, St. Petersburg (Heteroptera). Zoosystematica Rossica, 10 (2), 361–373.

    Dunn, C.P. (2003) Keeping taxonomy based in morphology. Trends in Ecology and Evolution, 18, 270–271.

    Dupuis, C. (1949) Les Asopinae de la faune Française (Hemiptera Pentatomidae). Essai sommaire de synthèse morphologique, systématique et biologique. Revue Française d’Entomologie, 16, 233–250.

    Esaki, T. (1952) Hemiptera: Heteroptera. In: Esaki, T., Ishii, T., Kawamura, T., Kinoshita, S., Kuwayama, S., Shiraki, T., Uchida, S. & Yuasa, H. (Eds.), Iconographia Insectorum Japonicorum. Editio secunda, reformata. Hokuryukan, Tokyo, pp. 185–270, pl. 1. [in Japanese]

    Esaki, T. & Ishihara, T. (1951) Hemiptera of Shansi, North China II. Pentatomoidea. Mushi, 22 (5), 29–44, pls. 5–7.

    Fabricius, J.C. (1794) Entomologia systematica emendata et aucta. Secundum classes, ordines, genera, species, adiectis synonimis [sic], locis, observationibus, descriptionibus. Tom. IV. Proft, Hafniae, 472 pp.

    Fallou, G. (1881) Hémiptéres nouveaux de la Chine. Le Naturaliste, 3 (43), 340–341.

    Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome coxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299.

    Frézal, L. & Leblois, R. (2008) Four years of DNA barcoding: current advances and prospects. Infection, Genetics and Evolution, 8 (5), 727–736.
    https://doi.org/10.1016/j.meegid.2008.05.005

    Gao, C.Q., Wang, Z.M. & Yu, E.Y. (1993) Studies on artificial rearing of Arma chinensis Fallou. Journal of Jilin Forest Science Technology, 2, 16–18. [in Chinese]

    Gao, Z. (2010) Studies on biological characteristic and control condition of Arma chinensis Fallou. Master Thesis, Heilongjiang University, Harbin, 52 pp. [in Chinese]

    Gao, Z., Wang, X.W., Zhang, X.L., Sun, Y., Fan, J.S. & Wang, G.Q. (2011) Biological characteristic of Arma chinensis. Journal of Engineering of Heilongjiang University, 2 (4), 72–77. [in Chinese]

    Gapon, D.A. & Konstantinov, F.V. (2006) On the structure of the aedeagus in shield bugs (Heteroptera, Pentatomidae): III. Subfamily Asopinae. Entomologicheskoe Obozrenie, 85 (3), 491–507.

    Gapud, V.P. (2015) The Philippine genus Stilbotes Stål and a new tribe of Asopinae (Hemiptera: Pentatomidae). Asia Life Sciences, 24 (2), 493–497.

    Glenister, C.S. (1998) Predatory heteropterans in augmentative biological control: an industry perspective. In: Coll, M. & Ruberson, J.R. (Eds.), Predatory Heteroptera: their ecology and use in biological control. Proceedings of the Thomas Say Publications in Entomology. Entomological Society of America, Lanham, MD, pp. 199–208.

    Hajibabaei, M., Singer, G.A.C., Hebert, P.D.N. & Hickey, D.A. (2007) DNA barcoding: how it complements taxonomy, molecular phylogenetics and population genetics. Trends in genetics, 23 (4), 167–172.

    https://doi.org/10.1016/j.tig.2007.02.001

    Hall, T. (2004) Bioedit7.0.0. Nucleic Carolina State University, Raleigh. [software]

    Hebert, P.D.N., Cywinska, A., Ball, S.L. & Dewaard, B.R. (2003a) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London Series B-Biological Sciences, 270, 313–321.
    https://doi.org/10.1098/rspb.2002.2218

    Hebert, P.D.N., Ratnasingham, S. & Dewaard, J.R. (2003b) Barcoding animal life: cytochrome oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London Series B Biological Sciences, 270, S96–S99.
    https://doi.org/10.1098/rsbl.2003.0025

    Hebert, P.D.N., Penton, E.H., Burns, J.M., Janzen, D.H. & Hallwachs, W. (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper, butterfly Astraptes fulgerator. PNAS, 101 (41), 14812–14817.
    https://doi.org/10.1073/pnas.0406166101

    Hoffmann, W.E. (1948) First supplement to catalogue of Scutelleroidea. Lingnan Science Journal, 4, 1–41.

    Hsiao, T.Y. (1977) A handbook for the determination of the Chinese Hemiptera- Heteroptera. Vol. 1. Science Press, Beijing, pp.116–141. [in Chinese]

    Hua, J.M., Li, M., Dong, P.Z., Cui, Y., Xie, Q. & Bu, W.J. (2008) Comparative and phylogenomic studies on the mitochondrial genomes of Pentatomomorpha (Insecta: Hemiptera: Heteroptera). BMC Genomics, 9, 610.
    https://doi.org/10.1186/1471-2164-9-610

    Jakovlev, V.E. (1902) Hémiptères-Hétéroptères nouveaux de la faune paléarctique. II. Revue Russe d’Entomologie, 2 (2), 63–70.

    Josifov, M.V. (1986) Über die Verbreitung mancher Heteropterenarten auf der Balkanhalbinsel und der Insel Zypern. Acta Zoologica Bulgarica, 31, 42–48.

    Josifov, M.V. & Kerzhner, I.M. (1978) Heteroptera aus Korea. II. Teil (Aradidae, Berytidae, Lygaeidae, Pyrrhocoridae, Rhopalidae, Alydidae, Coreidae, Urostylidae, Acanthosomatidae, Scutelleridae, Pentatomidae, Cydnidae, Plataspidae). Fragmenta Faunistica, 23 (9), 137–196.

    Jung, S., Duwal, R.K. & Lee, S. (2011) COI barcoding of true bugs (Insecta, Heteroptera). Molecular Ecology Resources, 11 (2), 266–270.

    Kiritshenko, A.N. (1922) Analecta hemipterologica. II. Revue Russe d’Entomologie, 18 (1), 8–19.

    Li, C.A., Han, F.Y., Zhang, M., Fu, C.Y., Du, Z.Z., Li, P.Y., Wang, Y.Z., Liu, Z.P. & Cheng, J.X. (1985) The Hemiptera Fauna Survey of Jigong Mountain Range in Henan. Journal of Shanxi University (Natural Science Edition), 3, 97–101.

    Li, Y. & Yao, G. (2015) Reinstatement and lectotypification of Bridelia fordii (Phyllanthaceae). Phytotaxa, 226, 295–297.
    https://doi.org/10.11646/phytotaxa.226.3.12

    Li, Y.J., Long, J., Zhang, S.M. & Zheng, L.Y. (2000) A checklist of species of Asopinae (Hemiptera: Pentatomoidea) from China. Jiangxi Plant Protection, 23 (2), 36–39. [in Chinese]

    Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25 (11), 1451–1452.
    https://doi.org/10.1093/bioinformatics/btp187

    Lipscomb, D., Platnick, N. & Wheeler, Q.D. (2003) The intellectual content of taxonomy: a comment on DNA taxonomy. Trends in Ecology and Evolution, 18, 65–66.

    Lis, J.A. (2000) Pluskwiaki różnoskrzydłe—Heteroptera. Tarczówkowate— Pentatomidae. In: Buszko, J. (Eds.), Klucze do oznaczania owadów Polski. 18 (14). Polish Entomological Society, Toruń, pp. 1–76. [in Polish]

    Lis, J.A., Lis, B. & Ziaja, D.J. (2016) In BOLD we trust? A commentary on the reliability of specimen identification for DNA barcoding: a case study on burrower bugs (Hemiptera: Heteroptera: Cydnidae). Zootaxa, 4114 (1), 83–86.
    https://doi.org/10.11646/zootaxa.4114.1.6

    Liu, H.M., Jiang, R.H., Guo, J., Hovenkamp, P., Perrie, L.R., Shepherd, L., Hennequin, S. & Schneider, H. (2013) Towards a phylogenetic classification of the climbing fern genus Arthropteris. Taxon, 62 (4), 688–700.
    https://doi.org/10.12705/624.26

    Mallott, E.K., Garber, P.A. & Malhi, R.S. (2017) Integrating feeding behavior, ecological data, and DNA barcoding to identify developmental differences in invertebrate foraging strategies in wild white-faced capuchins (Cebus capucinus). American Journal of Physical Anthropology, 162 (2), 241–254.

    Memon, N., Meier, R., Manan, A. & Su, K.F. (2006) On the use of DNA sequences for determining the species limits of a polymorphic new species in the stink bug genus Halys (Heteroptera: Pentatomidae) from Pakistan. Systematic Entomology, 31, 703–710.
    https://doi.org/10.1111/j.1365-3113.2006.00350.x

    Moritz, C. & Cicero, C. (2004) DNA barcoding: promise and pitfalls. PLoS Biology, 2, 1529–1531.
    https://doi.org/10.1371/journal.pbio.0020354

    Motschulsky, V. (1860) Catalogue des insectes rapportés des environs du fl. Amour, depuis la Schilka jusqu’à Nikolaëvsk, examinés et énumérés. Bulletin de la Société Impériale des Naturalistes de Moscou, 32 (4), 487–507.

    Negri, M., Pileggi, L.G. & Mantelatto, F.L. (2012) Molecular barcode and morphological analyses reveal the taxonomic and biogeographical status of the striped legged hermit crab species Clibanarius sclopetarius (Herbst, 1796) and Clibanarius vittatus (Bosc, 1802) (Decapoda: Diogenidae). Invertebrate Systematics, 26, 561–571.
    https://doi.org/10.1071/IS12020

    Nonnaizab (1988) Fauna of Inner Mongolia (Hemiptera: Heteroptera). Volume 1. Inner Mongolia People’s Publishing House, Hohhot, 469 pp. [in Chinese, English summary]

    Packer, L., Grixti, J.C., Roughley, R.E. & Hanner, R. (2009) The status of taxonomy in Canada and the impact of DNA barcoding. Canadian Journal of Zoology-Revue Canadienne De Zoologie, 87, 1097–1110.
    https://doi.org/10.1139/Z09-100

    Péricart, J. (2010) Hémiptères Pentatomoidea euro-méditerranéens. In: Faune de France, France et régions limitrophes. Vol. 3. Podopinae et Asopinae. Fédération Française des Sociétés de Sciences Naturelles, Paris, pp.1–293.

    Posada, D. & Crandall, K.A. (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817–818.

    Prendini, L. (2005) Comment on ‘Identifying spiders through DNA barcodes’. Canadian Journal of Zoology, 83, 498–504.
    https://doi.org/10.1139/z05-025

    Raupach, M.J., Hendrich, L., Küchler, S.M., Deister, F., Morinière, J. & Gossner, M.M. (2014) Building-up of a DNA Barcode Library for True Bugs (Instcta: Hemiptera: Heteroptera) of Germany Reveals Taxonomic Uncertainties and Surprises. PLoS ONE, 9 (9), e106940.
    https://doi.org/10.1371/journal.pone.0106940

    Remm, H. (1976) On rare insects from Moniste (south-eastern Estonia). Faunistilisi Markm, 2 (2), 1–2.

    Reuter, O.M. (1909) Charakteristik und Entwicklungsgeschichte der Hemipteren fauna (Heteroptera, Auchenorrhyncha und Psyllidae) der palaearktischen Coniferen. Acta Societatis Scientiarum Fennicae, 36 (1), 1–129.

    Riedel, A., Sagata, K., Suhardjono, Y.R., Tänzler, R., & Balke, M. (2013) Integrative taxonomy on the fast track-towards more sustainability in biodiversity research. Frontiers in Zoology, 10 (1), 15.

    Rider, D.A. (2006) Family Pentatomidae Leach, 1815. In: Aukema, B., Rieger, C.H.: Catalogue of the Heteroptera of the Palaearctic Region. Vol. 5. Pentatomomorpha II. The Netherlands Entomological Society, Amsterdam, pp. 233–402.

    Rider, D.A. & Zheng, L.Y. (2002) Checklist and nomenclatural notes on the Chinese Pentatomidae (Heteroptera) I, Asopinae. Entomotaxonomia, 24, 107–115.

    Ronquist, F. & Huelsenbeck, J.P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.

    Ronquist, F., Teslenko, M., Mark, P.V.D., Ayres, D.L., Darling, A. & Höhna, S. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61 (3), 539–542.
    https://doi.org/10.1093/sysbio/sys029

    Seidenstücker, G. (1975) Über anatolische Schildwanzen (Heteroptera, Pentatomidae). Reichenbachia, 15 (30), 259–268.

    Seidel, M. (2016) Morphology and DNA barcoding reveal a new species of Eudicella from East Africa (Coleoptera: Scarabaeidae: Cetoniinae). Zootaxa, 4137 (4), 535–544.

    Schindel, D.E. & Miller, S.E. (2005) DNA barcoding a useful tool for taxonomists. Nature, 35, 17.

    Schouteden, H. (1907) Heteroptera, fam. Pentatomidae, subfam. Asopinae (Amyoteinae). In: Wytsman, P. (Eds.), Genera Insectorum, 52, pp. 1–82, pls. 1–5.

    Schumacher, F. (1910) Beiträge zur Kenntnis der Biologie der Asopiden. Zeitschrift für Wissenschaftliche Insektenbiologie, 6, 430–437.

    Seberg, O.C., Humphries, J., Knapp, S., Stevenson, D.W., Petersen, G., Scharff, N. & Andersen, N.M. (2003) Shortcuts in systematics? A commentary on DNA-based taxonomy. Trends in Ecology and Evolution, 18, 63–65.
    https://doi.org/10.1016/S0169-5347(02)00059-9

    Shu, J.P., Shang, H., Jin, D., Wei, H.J., Zhou, X.L. & Liu, H.M. (2017) Re-establishment of species from synonymies based on DNA barcoding and phylogenetic analysis using Diplopterygium simulans (Gleicheniaceae) as an example. PLoS ONE, 12 (3), e0164604.
    https://doi.org/10.1371/journal.pone.0164604

    Stehlík, J.L. (1987) Results of the investigations on Hemiptera in Moravia made by the Moravian Museum (Pentatomoidea VI). Acta Musei Moraviae, Scientiae Naturales, 72, 183–201.

    Stehlík, J.L. & Vavřínová, I. (1994) Results of the investigations on Heteroptera in Slovakia made by the Moravian Museum (Pentatomoidea III). Acta Musei Moraviae, Scientiae Naturales, 78, 99–163.

    Stichel, W. (1961) Pentatomomorpha, Pentatomidae (partim), Acanthosomatidae, Cydnidae (partim). In: Stichel, W. (Ed.), Illustrierte Bestimmungstabellen der Wanzen. II. Europa. (Hemiptera-Heteroptera Europae). Vol. 4. Martin-Luther, Berlin-Hermsdorf, pp. 641–672.

    Swofford, D.L. (2003) PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts. [software]

    Szulczewski, A. (1913) Beitrag zu einem Verzeichnis der Posener Rhynchoten (Hemiptera). Deutsche Entomologische Zeitschrift, 1913, 307–314.

    Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis version6.0. Molecular biology evolution, 30 (12), 2725–2729.
    https://doi.org/10.1093/molbev/mst197

    Taylor, H.R. & Harris, W.E. (2012) An emergent science on the brink of irrelevance: a review of the past 8 years of DNA barcoding. Molecular ecology resource, 12, 377–388.
    https://doi.org/10.1111/j.1755-0998.2012.03119.x

    Thomas, D.B. (1994) Taxonomic synopsis of the Old World asopine genera (Heteroptera: Pentatomidae). Insecta Mundi, 8 (3–4), 145–212.

    Tolsgaard, S. (2001) Status over danske bredtæger, randtæger og ildtæger (Heteroptera: Pentatomoidea, Coreoidea & Pyrrhocoroidea). Entomologiske Meddelelser, 69, 3–46. [in Danish, English summary]

    Vidal, J.P. (1949) Hémiptères de l’Afrique du Nord et des Pays Circum-Méditerranéens. Mémoires de la Société des Sciences Naturelles du Maroc, 48, 1–238.

    Wagner, E. (1966) Eine Heteropterenausbeute aus der Türkei (Hemiptera, Heteroptera). Bulletin Des Recherches Agronomiques De Gembloux, 1 (4), 646–654.

    Wang, W.L., Liu, Q., Yan, J.H., Kang, Z., Lin, Z.Q. & Zhang, X.H. (2012) Preliminary observation of preyed ability of Arma chinensis (Fallou), a new natural enemy of Hyphantria cunea (Drury). Shandong Forest Science Technology, 1, 11–14.

    Will, K.W. & Rubinoff, D. (2004) Myth of the molecule: DNA barcodes for species cannot replace morphology for identification and classification. Cladistics, 20, 47–55.
    https://doi.org/10.1111/j.1096-0031.2003.00008.x

    Yang, W.I. (1933) Notes on some species of Pentatomidae from N. China. Bulletin of the Fan Memorial Institute of Biology, Zoology, 4 (2), 9–46.

    Yang, W.I. (1934) Notes on the Chinese Asopinae (Heteroptera, Pentatomidae). Sinensia, 5 (2), 92–121.

    Yang, W.I. (1962) Hemiptera, Pentatomidae. In: Economic Insect Fauna of China. Vol. 2. Academia Sinica, Science Press, Beijing, 138 pp., 10 pls.

    Zhang, S.M. & Lin, Y.J. (1987) Hemiptera [sic]: Pentatomidae. In: Zhang, S.M. (Ed.), Agricultural insects, spiders, plant diseases and weeds of Xizang. Vol. 1. Xizang People’s Publishing House, Lhasa, pp. 75–83. [in Chinese, English summary]

    Zhao, Q., Liu, G.Q. & Bu, W.J. (2013a) A review of the genus Picromerus Amyot and Serville from China, with description of a new species (Heteroptera: Pentatomidae: Asopinae). Zootaxa, 3613 (2), 146–164.

    Zhao, Q., Rédei, D. & Bu, W.J. (2013b) A revision of the genus Pinthaeus (Hemiptera: Heteroptera: Pentatomidae: Asopinae). Zootaxa, 3636 (1), 36–84.

    Zhao, W.Q., Zhao, Q., Li, M., Wei, J.F., Zhang, X.X. & Zhang, H.F. (2017) DNA Barcoding of Chinese species of the genus Eurydema Laporte, 1833 (Hemiptera: Pentatomidae). Zootaxa, 4286 (2), 151–175.
    https://doi.org/10.11646/zootaxa.4286.2.1

    Zheng, L.Y. (1981) Chinese species of genus Arma Hahn (Hemiptera: Pentatomidae). Natural Enemies of Insects, 3, 28–32. [in Chinese]

    Zou, D.Y., Wang, M.Q., Zhang, L.S., Zhang, Y., Zhang, X.J. & Chen, H.Y. (2012) Taxonomic and bionomic notes on Arma chinensis (Fallou) (Hemiptera: Pentatomidae: Asopinae). Zootaxa, 3382, 41–52.