Eur. J. Entomol. 115: 512-523, 2018 | DOI: 10.14411/eje.2018.051

Survey and DNA barcoding of flat bugs (Hemiptera: Aradidae) in the Tanzanian Forest Archipelago reveal a phylogeographically structured fauna largely unknown at the species levelOriginal article

Vasily V. GREBENNIKOV1, Ernst HEISS2
1 Canadian Food Inspection Agency, K.W. Neatby Building, 960 Carling Ave., Ottawa, ON, K1A 0C6, Canada; e-mail: vasily.grebennikov@canada.ca
2 Tiroler Landesmuseum, Josef-Schraffl-Strasse 2a, A-6020 Innsbruck, Austria; e-mail: aradus@aon.at

We report results of a faunal survey of Aradidae flat bugs sampled by sifting litter in 14 wet and discrete Tanzanian primary forests (= Tanzanian Forest Archipelago, TFA) of different geological origins and ages. Images, locality data and, when available, DNA barcoding sequences of 300 Aradidae adults and nymphs forming the core of the herein analyzed data are publicly available online at dx.doi.org/10.5883/DS-ARADTZ. Three Aradidae subfamilies and seven genera were recorded: Aneurinae (Paraneurus), Carventinae (Dundocoris) and Mezirinae (Afropictinus, Embuana, Linnavuoriessa, Neochelonoderus, Usumbaraia); the two latter subfamilies were also represented by specimens not assignable to nominal genera. Barring the six nominal species of Neochelonoderus and Afropictinus described earlier by us from these samples and representing 11 of the herein defined Operational Taxonomic Units (OTU), only one of the remaining 52 OTUs could be assigned to a named species; the remaining 51 OTUs (81%) represent unnamed species. Average diversity of Aradidae is 4.64 species per locality; diversity on the three geologically young volcanoes (Mts Hanang, Meru, Kilimanjaro) is significantly lower (1.33) than on the nine Eastern Arc Mountains (5.67) and in two lowland forests (5). Observed phylogeographic structure of Aradidae in TFA can be attributed to vicariance, while the depauperate fauna of Aradidae on geologically young Tanzanian volcanoes was likely formed anew by colonisation from nearby and geologically older forests.

Keywords: Heteroptera, Aradidae, Mezirinae, microptery, Tanzania, barcoding, phylogeography, Eastern Arc Mountains

Received: May 4, 2018; Revised: August 15, 2018; Accepted: August 15, 2018; Published online: September 26, 2018  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
GREBENNIKOV, V.V., & HEISS, E. (2018). Survey and DNA barcoding of flat bugs (Hemiptera: Aradidae) in the Tanzanian Forest Archipelago reveal a phylogeographically structured fauna largely unknown at the species level. EJE, 115, Article 512-523. https://doi.org/10.14411/eje.2018.051
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    Attachments

    Download fileEJE_115_512_Grebennikov_S01.pdf

    File size: 3.9 MB

    References

    1. Baòaø P. & Heiss E. 2018: A new species of Comorocoris from Northern Madagascar (Hemiptera: Heteroptera: Aradidae). - Zootaxa 4375: 433-440. Go to original source...
    2. Brokent A., Brown B.V., Adler P.H., Amorim D.S., Barber K., Bickel D., Boucher S., Brooks S.E., Burger J., Burington Z.L. et al. 2018: Remarkable fly (Diptera) diversity in a patch of Costa Rican cloud forest: why inventory is a vital science. - Zootaxa 4422: 53-90. Go to original source...
    3. Cassis G. & Schuh R.T. 2010: Systematic methods, fossils, and relationships within Heteroptera (Insecta). - Cladistics 26: 262-280. Go to original source...
    4. Chérot F., Aukema B., Bruers J. & Viskens G. 2011: Exotic species of Aradidae and Miridae (Insecta: Hemiptera, Heteroptera) recently found in Antwerp Harbour, Belgium. - Bull. Soc. R. Belge Entomol. 147: 14-19.
    5. Collins R.A. & Cruickshank R.H. 2013: The seven deadly sins of DNA barcoding. - Mol. Ecol. Res. 13: 969-975. Go to original source...
    6. deMenocal P.B. 2004: African climate change and faunal evolution during the Pliocene-Pleistocene. - Earth Planet. Sci. Lett. 220: 3-24. Go to original source...
    7. Grazia J., Schuh R.T. & Wheeler W.C 2008: Phylogenetic relationships of family groups in Pentatomoidea basedon morphology and DNA sequences (Insecta: Heteroptera). - Cladistics 24: 932-976. Go to original source...
    8. Grebennikov V.V. 2017: Phylogeography and sister group of Lupangus, a new genus for three new flightless allopatric forest litter weevils endemic to the Eastern Arc Mountains, Tanzania (Coleoptera: Curculionidae, Molytinae). - Fragm. Entomol. 49: 37-55. Go to original source...
    9. Grebennikov V.V. & Heiss E. 2014: DNA barcoding of flat bugs (Hemiptera: Aradidae) with phylogenetic implications. - Arthr. Syst. Phylogeny 72: 213-219. Go to original source...
    10. Grebennikov V.V., Jendek E. & Smirnov M.E. 2017: Diagnostic and phylogenetic utility of the first DNA barcode library for longhorn beetles (Coleoptera: Cerambycidae) from the Russian Far East. - Zootaxa 4276: 441-445. Go to original source...
    11. Felsenstein J. 1985: Confidence limits on phylogenies: an approach using the bootstrap. - Evolution 39: 783-791. Go to original source...
    12. Funk D.J. & Omland K.E. 2003: Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. - Annu. Rev. Ecol. Evol. Syst. 34: 397-423. Go to original source...
    13. Hamilton A.C. & Taylor D. 1991: History of climate and forests in tropical Africa during the last 8 million years. - Clim. Change 19: 65-78. Go to original source...
    14. Havemann N., Gossner M.M., Hendrich L., Morinière J., Niedringhaus R., Schäfer P. & Raupach M.J. 2018: From water striders to water bugs: the molecular diversity of aquatic Heteroptera (Gerromorpha, Nepomorpha) of Germany based on DNA barcodes. - PeerJ 6: e4577, 30 pp. Go to original source...
    15. Heads M. 2014: Biogeography of Australasia. A Molecular Analysis. Cambridge University Press, Cambridge, 503 pp. Go to original source...
    16. Hebert P.D.N., Cywinska A., Ball S.L. & DeWaard J.R. 2003a: Biological identifications through DNA barcodes. - Proc. R. Soc. (B) 270: 313-321. Go to original source...
    17. Hebert P.D.N., Ratnasingham S. & DeWaard J.R. 2003b: Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. - Proc. R. Soc. (B) 270: 96-99. Go to original source...
    18. Heiss E. 2012: Annotated catalogue of the flat bug family Aradidae Brullé, 1836 of Madagascar and adjacent islands (Hemiptera: Heteroptera). - Zootaxa 3426: 45-63. Go to original source...
    19. Heiss E. 2013: Annotated checklist of the flat bug family Aradidae Brullé, 1836 from East Africa (Hemiptera, Heteroptera). - Zootaxa 3718: 331-344. Go to original source...
    20. Heiss E. & Baòaø P. 2016: Two new genera of micropterous Mezirinae from Kenya (Hemiptera: Heteroptera: Aradidae). - Entomol. Amer. 122: 18-23. Go to original source...
    21. Heiss E. & Grebennikov V.V. 2015: Review and three new species of the flat bug genus Neochelonoderus Hoberlandt, 1967 from East Africa (Hemiptera: Heteroptera: Aradidae). - Zootaxa 3947: 581-589. Go to original source...
    22. Heiss E. & Grebennikov V.V. 2016: Monophyly, review, six new species and DNA barcode of micropterous Afromontane Afropictinus (Heteroptera: Aradidae). - Zootaxa 4208: 149-160. Go to original source...
    23. Hendrich L., Morinière J., Haszprunar G., Hebert P.D.N, Hausmann A., Köhler F. & Balke M. 2015: A comprehensive DNA barcode database for Central European beetles with a focus on Germany: adding more than 3500 identified species to BOLD. - Mol. Ecol. Res. 15: 795-818. Go to original source...
    24. Ivanova N.V., DeWaard J.R. & Hebert P.D.N. 2006: An inexpensive, automation-friendly protocol for recovering high-quality DNA. - Mol. Ecol. Notes 6: 998-1002. Go to original source...
    25. Ivanova N.V., deWaard J.R., Hajibabaei M. & Hebert P.D.N. 2014: Protocols for high-volume DNA barcode analysis. URL: https://www.researchgate.net/profile/Paul_Hebert2/publication/238509959_Protocols_for_High-Volume_DNA_Barcode_Analysis/links/53d169190cf220632f393902/Protocols-for-High-Volume-DNA-Barcode-Analysis.pdf?origin=publication_detail
    26. Jacobs D.H. 1986: Morphology and taxonomy of sub-saharan Aneurus species with notes on their phylogeny, biology and cytogenetics (Heteroptera: Aradidae: Aneurinae). - Entomol.Mem. Dep. Agric. Tech. Tech. Serv. Rep. S. Afr. 64: 1-45.
    27. Kormilev N.A. & Froeschner R.C. 1987: Flat bugs of the World. A synonymic list (Heteroptera: Aradidae). - Entomography 5: 245 pp.
    28. Larivière M.-C. & Larochelle A. 2006: An overview of flat bug genera (Hemiptera, Aradidae) from New Zealand, with considerations of faunal diversification and affinities. - Denisia 9: 181-214.
    29. Lees D.C., Kawahara A.Y., Rougerie R., Ohshima I., Kawakita A., Bouteleux O, De Prins J. & Lopez-Vaamonde C. 2014: DNA barcoding reveals a largely unknown fauna of Gracillariidae leaf-mining moths in the Neotropics. - Mol. Ecol. Res. 14: 289-296. Go to original source...
    30. Liu Y., Song F., Jiang P., Wilson J.-J., Cai W. & Li H. 2018: Compositional heterogeneity in true bug mitochondrial phylogenomics. - Mol. Phylogenet. Evol. 118: 135-144. Go to original source...
    31. Lovett J.C. & Wasser S.K. (eds) 1993: Biogeography and Ecology of the Rain Forests of Eastern Africa. Cambridge University Press, Cambridge, 341 pp. Go to original source...
    32. Marchal L. & Guilbert E. 2015: Cladistic analysis of Aradidae (Insecta, Heteroptera) based on morphological and molecular characters. - Zool. Scr. 45: 273-285. Go to original source...
    33. Miller M., Pfeiffer W. & Schwartz T. 2010: Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA. pp. 1-8. Go to original source...
    34. Monteith G.B. 1997: Revision of the Australian flat bugs of the subfamily Mezirinae (Insecta: Hemiptera: Aradidae). - Mem. Qld Mus. 41: 1-169.
    35. Newmark W.D. 2002: Conserving Biodiversity in East African Forests: A study of the Eastern Arc Mountains. Ecological Studies 155. Springer, Berlin, 205 pp. Go to original source...
    36. Nonnotte P., Guillou H., Le Gall B., Benoit M., Cotton J. & Scaillet S. 2008: New K-Ar age determinations of Kilimanjaro volcano in the North Tanzanian diverging rift, East Africa. - J. Volcanol. Geotherm. Res. 173: 99-112. Go to original source...
    37. Popper K. 1959: The Logic of Scientific Discovery. Basic Books, New York, 484 pp.
    38. Rambaut A. 2014: FigTree, Version 1.4. URL: http://tree.bio.ed.ac.uk/software/figtree/ (last accessed 12 Mar. 2014).
    39. 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 (Insecta: Hemiptera: Heteroptera) of Germany reveals taxonomic uncertainties and surprises. - PLoS One 9: e106940, 13 pp. Go to original source...
    40. Ratnasingham S. & Hebert P.D.N. 2007: BOLD: The Barcode of Life Data System (http://www. barcodinglife. org). - Mol. Ecol. Notes 7: 355-364. Go to original source...
    41. Ratnasingham S. & Hebert P.D.N. 2013: A DNA-based registry for all animal species: the Barcode Index Number (BIN) system. - PLoS ONE 8: e66213, 16 pp. Go to original source...
    42. Rougerie R., Kitching I.J., Haxaire J., Miller S.E., Hausmann A. & Hebert P.D.N. 2014: Australian Sphingidae - DNA barcodes challenge current species boundaries and distributions. - PLoS ONE 9(7): e101108, 12 pp. Go to original source...
    43. Schmidt S., Schmid-Egger C., Morinière J., Haszprunar G. & Hebert P.D.N. 2015: DNA barcoding largely supports 250 years of classical taxonomy: identifications for Central European bees (Hymenoptera, Apoidea partim). - Mol. Ecol. Res. 15: 985-1000. Go to original source...
    44. Schuh R.T. & Slater J.A. 1995: True Bugs of the World (Hemiptera: Heteroptera): Classification and Natural History. Cornell University Press, Ithaca, NY, 336 pp.
    45. Shorthouse D.P. 2010: SimpleMappr, an Online Tool to Produce Publication-Quality Point Maps. URL: http://www.simplemappr.net
    46. Song F., Li H., Shao R., Shi A., Bai X., Zheng X., Heiss E. & Cai W. 2016: Rearrangement of mitochondrial tRNA genes in flat bugs (Hemiptera: Aradidae). - Sci. Rep. 6: 25725, 9 pp. Go to original source...
    47. Smith-Pardo A.H. & Beucke K. 2015: Flat Bugs (Hemiptera: Heteroptera: Aradidae) intercepted at United States ports of entry. - Pan-Pac. Entomol. 91: 58-81. Go to original source...
    48. Stamatakis A., Hoover P. & Rougemont J. 2008: A rapid bootstrap algorithm for the RAxML web servers. - Syst. Biol. 57: 758-771. Go to original source...
    49. Usinger R.L. & Matsuda R. 1959: Classification of the Aradidae. British Museum of Natural History, London, 410 pp.
    50. Vences M., Guayasamin J.M., Miralles A. & De La Riva I. 2013: To name or not to name: criteria to promote economy of change in Linnaean classification schemes. - Zootaxa 3636: 201-244. Go to original source...
    51. Ward P.S. 2011: Integrating molecular phylogenetic results into ant taxonomy (Hymenoptera: Formicidae). - Myrmecol. News 15: 21-29.
    52. Wilson J.J., Rougerie R., Schonfeld J., Janzen D.H., Hallwachs W., Hajibabaei M., Kitching I.J., Haxaire J. & Hebert P.D.N. 2011: When species matches are unavailable are DNA barcodes correctly assigned to higher taxa? An assessment using sphingid moths. - BMC Ecol. 11: 18, 14 pp. Go to original source...
    53. Usinger R.L. & Matsuda R. 1959: Classification of the Aradidae (Hemiptera - Heteroptera). British Museum of Natural History, London, 410 pp.
    54. Yao Y., Ren D., Rider D.A. & Cai W. 2012: Phylogeny of the infraorder Pentatomomorpha based on fossil and extant morphology, with description of a new fossil family from China. - PLoS ONE 7(5): e37289, 17 pp. Go to original source...
    55. Yoder A.D. & Nowak M.D. 2006: Has vicariance or dispersal been the predominant biogeographic force in Madagascar? Only time will tell. - Annu. Rev. Ecol. Evol. Syst. 37: 405-431. Go to original source...
    56. Zahiri R., Lafontaine J.D., Schmidt C.C., Zakharov E.V. & Hebert P.D.N. 2017: Probing planetary biodiversity with DNA barcodes: The Noctuoidea of North America. - PLoS ONE 12: e0178548, 18 pp. Go to original source...

    This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.


    Return to the content