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Morphological identification and COI barcodes of adult flies help determine species identities of chironomid larvae (Diptera, Chironomidae)

Published online by Cambridge University Press:  15 June 2015

A.J. Failla ,
A.A. Vasquez ,
P. Hudson ,
M. Fujimoto  and
J.L. Ram
A.J. Failla
Affiliation:
Department of Physiology, Wayne State University School of Medicine, 5374 Scott Hall, 540 E. Canfield St., Detroit, MI 48201
A.A. Vasquez
Affiliation:
Department of Physiology, Wayne State University School of Medicine, 5374 Scott Hall, 540 E. Canfield St., Detroit, MI 48201
P. Hudson
Affiliation:
Great Lakes Science Center, U.S. Geological Survey, 1451 Green Road, Ann Arbor, MI 48105, USA
M. Fujimoto
Affiliation:
Department of Physiology, Wayne State University School of Medicine, 5374 Scott Hall, 540 E. Canfield St., Detroit, MI 48201
J.L. Ram*
Affiliation:
Department of Physiology, Wayne State University School of Medicine, 5374 Scott Hall, 540 E. Canfield St., Detroit, MI 48201
*
*Author for correspondence Phone: 1-313-577-1558 Fax: 1-267-345-9684 E-mail: [email protected]
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Abstract

Establishing reliable methods for the identification of benthic chironomid communities is important due to their significant contribution to biomass, ecology and the aquatic food web. Immature larval specimens are more difficult to identify to species level by traditional morphological methods than their fully developed adult counterparts, and few keys are available to identify the larval species. In order to develop molecular criteria to identify species of chironomid larvae, larval and adult chironomids from Western Lake Erie were subjected to both molecular and morphological taxonomic analysis. Mitochondrial cytochrome c oxidase I (COI) barcode sequences of 33 adults that were identified to species level by morphological methods were grouped with COI sequences of 189 larvae in a neighbor-joining taxon-ID tree. Most of these larvae could be identified only to genus level by morphological taxonomy (only 22 of the 189 sequenced larvae could be identified to species level). The taxon-ID tree of larval sequences had 45 operational taxonomic units (OTUs, defined as clusters with >97% identity or individual sequences differing from nearest neighbors by >3%; supported by analysis of all larval pairwise differences), of which seven could be identified to species or ‘species group’ level by larval morphology. Reference sequences from the GenBank and BOLD databases assigned six larval OTUs with presumptive species level identifications and confirmed one previously assigned species level identification. Sequences from morphologically identified adults in the present study grouped with and further classified the identity of 13 larval OTUs. The use of morphological identification and subsequent DNA barcoding of adult chironomids proved to be beneficial in revealing possible species level identifications of larval specimens. Sequence data from this study also contribute to currently inadequate public databases relevant to the Great Lakes region, while the neighbor-joining analysis reported here describes the application and confirmation of a useful tool that can accelerate identification and bioassesment of chironomid communities.

Keywords

ChironomidaeDNA barcodingspecies-level identificationmorphologyGreat Lakes
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 106 , Issue 1 , February 2016 , pp. 34 - 46
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Copyright
Copyright © Cambridge University Press 2015 

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References

Abbott, R., Albach, D., Ansell, S., Arntzen, J.W., Baird, S.J.E., Bierne, N., Boughman, J., Brelsford, A., Buerkle, C.A., Buggs, R., Butlin, R.K., Dieckmann, U., Eroukhmanoff, F., Grill, A., Cahan, S.H., Hermansen, J.S., Hewitt, G., Hudson, A.G., Jiggins, C., Jones, J., Keller, B., Marczewski, T., Mallet, J., Martinez-Rodriguez, P., Möst, M., Mullen, S., Nichols, R., Nolte, A.W., Parisod, C., Pfennig, K., Rice, A.M., Ritchie, M.G., Seifert, B., Smadja, C.M., Stelkens, R., Szymura, J.M., Väinölä, R., Wolf, J.B.W. & Zinner, D. (2013) Hybridization and speciation. Journal of Evolutionary Biology 26, 229–246.CrossRefGoogle ScholarPubMed
Ali, A. (1996) A concise review of chironomid midges (Diptera: Chironomidae) as pests and their management. Journal of Vector Ecology 21, 105–121.Google Scholar
Ali, A., Stanley, B.H. & Majori, G. (1985) Daily abundance patterns of pestiferous Chironomidae (Diptera) in an urban lakefront in central Florida. Environmental Entomology 14, 780–784.CrossRefGoogle Scholar
Anderson, A.M., Stur, E. & Ekrem, T. (2013) Molecular and morphological methods reveal cryptic diversity and three new species of Nearctic Micropsectra (Diptera: Chironomidae). Freshwater Science 32, 892–921.CrossRefGoogle Scholar
Armitage, P.D., Cranston, P.S. & Pinder, L.C.V. (1995) The Chironomidae: Biology and Ecology of Non-Biting Midges. London, Chapman and Hall.CrossRefGoogle Scholar
Bergsten, J., Bilton, D.T., Fujisawa, T., Elliott, M., Monaghan, M.T., Balke, M., Hendrich, L., Geijer, J., Herrmann, J., Foster, G.N., Ribera, I., Nilsson, A.N., Barraclough, T.G. & Vogler, A.P. (2012) The effect of geographical scale of sampling on DNA barcoding. Systematic Biology 61, 851–869.CrossRefGoogle ScholarPubMed
Broza, M., Halpern, M., Gahanma, L. & Inbar, M. (2003) Nuisance chironomids in waste water stabilization ponds: monitoring and action threshold assessment based on public complaints. Journal of Vector Ecology 28, 31–36.Google ScholarPubMed
Carew, M.E., Pettigrove, V. & Hoffmann, A.A. (2005) The utility of DNA markers in classical taxonomy: using cytochrome oxidase I markers to differentiate australian Cladopelma (Diptera: Chironomidae) midges. Annals of the Entomological Society of America 98, 587–594.CrossRefGoogle Scholar
Carew, M.E., Marshall, S.E. & Hoffmann, A.A. (2011) A combination of molecular and morphological approaches resolves species in the taxonomically difficult genus Procladius Skuse (Diptera: Chironomidae) despite high intra-specific morphological variation. Bulletin of Entomological Research 101, 505–519.CrossRefGoogle ScholarPubMed
Carr, J.F. & Hiltunen, J.K. (1965) Changes in the bottom fauna of Western Lake Erie from 1930 to 1961. Limnology and Oceanography 10, 551–569.CrossRefGoogle Scholar
Clement, S., Grigarick, A. & Way, M. (1977) The colonization of California rice paddies by chironomid midges. Journal of Applied Ecology 14, 379–389.CrossRefGoogle Scholar
Cranston, P.S., Dillon, M.E., Pinder, L.C.V. & Reiss, F. (1989) The adult males of Chironominae (Diptera, Chironomidae) of the Holarctic region – keys and diagnoses. Entomologica Scandinavica 34, 353–502.Google Scholar
Dendy, J.S. & Sublette, J.E. (1959) The Chironomidae (=Tendipedidae: Diptera) of Alabama with descriptions of six new species. Annals of the Entomological Society of America 52, 506–519.CrossRefGoogle Scholar
Ekrem, T., Willassen, E. & Stur, E. (2007) A comprehensive DNA sequence library is essential for identification with DNA barcodes. Molecular Phylogenetics and Evolution 43, 530–542.CrossRefGoogle ScholarPubMed
Ekrem, T., Willassen, E. & Stur, E. (2010) Phylogenetic utility of five genes for dipteran phylogeny: a test case in the Chironomidae leads to generic synonymies. Molecular Phylogenetic and Evolution 57, 561–571.Google ScholarPubMed
Epler, J.H. (1988) Biosystematics of the genus Dicrotendipes Kieffer, 1913 (Diptera: Chironomidae: Chironominae) of the world. Memoirs of the American Entomological Society 36, 1–214.Google Scholar
Failla, A.J., Vasquez, A.A., Fujimoto, M. & Ram, J.L. (2015) The ecological, economic and public health impacts of nuisance chironomids and their potential as aquatic invaders. Aquatic invasions 10, 1–15.CrossRefGoogle Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google ScholarPubMed
Golygina, V.V. & Kiknadze, II. (2012) A revision of chromosome II (CD) mapping in Chironomus plumosus (Linnaeus, 1758) group (Diptera, Chironomidae). Comparitive Cytogenetics 6, 249–266.Google ScholarPubMed
Gresens, S., Stur, E. & Ekrem, T. (2012) Phenotypic and genetic variation within the Cricotopus sylvestris species-group (Diptera, Chironomidae), across a Nearctic – Palaearctic gradient. Fauna norvegica 31, 137–149.CrossRefGoogle Scholar
Hebert, P.D., Cywinska, A., Ball, S.L. & deWaard, J.R. (2003 a) Biological identifications through DNA barcodes. Proceedings of the Biological Sciences 270, 313–321.CrossRefGoogle ScholarPubMed
Hebert, P.D.N., Ratnasingham, S. & de Waard, J.R. (2003 b) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London. Series B: Biological Sciences 270, S96–S99.CrossRefGoogle ScholarPubMed
Heyn, M. (1992) A review of the systematic position of the North American species of the genus Glyptotendipes . Netherland Journal of Aquatic Ecology 26, 129–137.CrossRefGoogle Scholar
Hirabayashi, K. & Okino, T. (1998) Massive flights of chironomid midge nuisance insects around a hypereutrophic lake in Japan: a questionnaire survey of tourists. Journal of the Kansas Entomological Society 71, 439–446.Google Scholar
Ilyashuk, B. & Ilyashuk, E. (2001) Response of alpine chironomid communities (Lake Chuna, Kola Peninsula, northwestern Russia) to atmospheric contamination. Journal of Paleolimnology 25, 467–475.Google Scholar
Inoue, E., Kimura, G., Denda, M., Tokioka, T., Tsushima, K., Amano, K. & Hirabayashi, K. (2008) Utility of larval rearing for assessment of lotic chironomid assemblages: a case study in a riffle/pool section of the middle reaches of the Shinano River, Japan. Boletim do Museu Municipal do Funchal 13, 119–126.Google Scholar
Iwakuma, T. (1992) Emergence of Chironomidae from the shallow eutrophic Lake Kasumigaura, Japan. Hydrobiologia 245, 27–40.CrossRefGoogle Scholar
Kiknadze, I.I., Butler, M.G., Golygina, V.V., Martin, J., Wulker, W.F., Sublette, J.E. & Sublette, M.F. (2000) Intercontinental karyotypic differentiation of Chironomus entis Shobanov, a Holarctic member of the C. plumosus group (Diptera, Chironomidae). Genome 43, 857–873.Google Scholar
Langton, P., Cranston, P. & Armitage, P. (1988) The parthenogenetic midge of water supply systems, Paratanytarsus grimmii (Schneider) (Diptera: Chironomidae). Bulletin of Entomological Research 78, 317–328.CrossRefGoogle Scholar
Langdon, P.G., Ruiz, Z., Brodersen, K.P. & Foster, I.D.L. (2006) Assessing lake eutrophication using chironomids: understanding the nature of community response in different lake types. Freshwater Biology 51, 562–577.CrossRefGoogle Scholar
Martin, J., Sublette, J.E. & Caldwell, B.A. (2011) Description of Chironomus quinnitukqut, n. sp., closely related to the C. decorus group in North America, with characterization of an additional larval form from halobiontic habitats. Zootaxa 2716, 29–41.CrossRefGoogle Scholar
Michailova, P. & Fischer, J. (1986) Speciation within the plumosus group of the genus Chironomus Meigen (Diptera, Chironomidae). Journal of Zoological Systematics and Evolutionary Research 24, 207–222.CrossRefGoogle Scholar
Oliver, D. (1971) Life history of the Chironomidae. Annual Review of Entomology 16, 211–230.Google Scholar
Olsen, A., Leadbeater, B.S., Callow, M.E., Holden, J.B. & Bale, J.S. (2009) The origin and population dynamics of annually re-occurring Paratanytarsus grimmii (Diptera: Chironomidae) colonising granular activated carbon (GAC) adsorbers used in potable water treatment. Bulletin of Entomological Research 99, 643–651.CrossRefGoogle ScholarPubMed
Pfenninger, M., Nowak, C., Kley, C., Steinke, D. & Streit, B. (2007) Utility of DNA taxonomy and barcoding for the inference of larval community structure in morphologically cryptic Chironomus (Diptera) species. Molecular Ecology 16, 1957–1968.CrossRefGoogle ScholarPubMed
Proulx, I., Martin, J., Carew, M. & Hare, L. (2013) Using various lines of evidence to identify Chironomus species (Diptera: Chironomidae) in eastern Canadain lakes. Zootaxa 3741, 401–458.CrossRefGoogle Scholar
Proviz, V.I. (2008) Speciation and chromosomal evolution of the Baikalian endemic chironomids of the genus Sergentia Kief. (Diptera, Chironomidae): Karyotype divergence and chromosomal polymorphism in the populations of eurybathic species Sergentia flavodentata Tshern. and littoral species Sergentia baicalensis Tshern. Russian Journal of Genetics 44, 1037–1048.CrossRefGoogle ScholarPubMed
Proviz, V.I. & Bazova, N.V. (2013) Karyotypic features of Chironomus entis and Chironomus borokensis (Diptera, Chironomidae) from Lake Kotokel (Lake Baikal Basin). Entomological Review 93, 35–44.CrossRefGoogle Scholar
Ram, J.L., Banno, F., Gala, R.R., Gizicki, J.P. & Kashian, D.R. (2014) Estimating sampling effort for early detection of non-indigenous benthic species in the Toledo harbor region of Lake Erie. Management of Biological Invasions 5, 209–216.CrossRefGoogle Scholar
Roback, S.S. (1971) The adults of the subfamily Tanypodinae (=Pelopiinae) in North America (Diptera: Chironomidae). Academy of Natural Sciences of Philadelphia Monographs 17, 1–410.Google Scholar
Saether, O.A. (1979) Chironomid communities as water quality indicators. Holarctic Ecology 2, 65–74.Google Scholar
Saether, O.A. (2009) Cryptochironomus Kieffer from Lake Winnipeg, Canada, with a review of Nearctic species (Diptera: Chironomidae). Zootaxa 2208, 1–24.CrossRefGoogle Scholar
Saether, O.A. (2011) Glyptotendipes Kieffer and Demeijerea Kruseman from Lake Winnipeg, Manitoba, Canada, with the description of four new species (Diptera: Chironomidae). Zootaxa 2760, 39–52.CrossRefGoogle Scholar
Sharley, D.J., Pettigrove, V. & Parsons, Y.M. (2004) Molecular identification of Chironomus spp. (Diptera) for biomonitoring of aquatic ecosystems. Australian Journal of Entomology 43, 359–365.Google Scholar
Silva, F.L. & Wiedenbrug, S. (2014) Integrating DNA barcodes and morphology for species delimitation in the Corynoneura group (Diptera: Chironomidae: Orthocladiinae). Bulletin of Entomological Research 104, 65–78.CrossRefGoogle ScholarPubMed
Silva, F.L.d., Ekrem, T. & Fonseca-Gessner, A.A. (2013) DNA barcodes for species delimitation in Chironomidae (Diptera): a case study on the genus Labrundinia . The Canadian Entomologist 145, 589–602.CrossRefGoogle Scholar
Sinclair, C.S. & Gresens, S.E. (2008) Discrimination of Cricotopus species (Diptera: Chironomidae) by DNA barcoding. Bulletin of Entomological Research 98, 555–563.Google ScholarPubMed
Tabaru, Y., Moriya, K. & Ali, A. (1987) Nuisance midges (Diptera, Chironomidae) and their control in Japan. Journal of the American Mosquito Control Association 3, 45–49.Google ScholarPubMed
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.CrossRefGoogle ScholarPubMed
Townes, H.K. Jr., (1945) The Nearctic species of Tendipedini [Diptera, Tendipedidae (=Chironomidae)]. American Midland Naturalist 34, 1–206.CrossRefGoogle Scholar
White, B.P., Pilgrim, E.M., Boykin, L.M., Stein, E.D. & Mazor, R.D. (2013) Comparison of four species-delimitation methods applied to a DNA barcode data set of insect larvae for use in routine bioassessment. Freshwater Science 33, 338–348.CrossRefGoogle Scholar