Revealing secret liaisons: DNA barcoding changes our understanding of food webs

Ecological Entomology

Volumn 35, Issue 5, 2010, Pages 623-638

  Kaartinen, Riikka ^a   Stone, Graham N ^b   Hearn, Jack ^b   Lohse, Konrad ^b   Roslin, Tomas ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Cryptic species; Food web structure; Herbivore community; Interaction evenness; Misidentification; MOTU; Parasitoids; Quantitative food web

Indexed keywords

BIOMARKER; FOOD WEB; GENETIC ANALYSIS; HERBIVORE; IDENTIFICATION METHOD; MORPHOLOGY; NATURAL ENEMY; PARASITOID; SPECIALIZATION; TROPHIC INTERACTION;

EID: 77956417431     PISSN: 03076946     EISSN: 13652311     Source Type: Journal    
DOI: 10.1111/j.1365-2311.2010.01224.x     Document Type: Article

References (98)

1. Ács Z, Challis R, Bihari P, Blaxter M, Hayward A, Melika G. Phylogeny and DNA barcoding of inquiline oak gallwasps (Hymenoptera: Cynipidae) of the Western Palaearctic. Molecular Phylogenetics and Evolution 2010, 55:210-225.
2. Albrecht M, Duelli P, Schmid B, Müller CB. Interaction diversity within quantified insect food webs in restored and adjacent intensively managed meadows. Journal of Animal Ecology 2007, 76:1015-1025.
3. Askew RR. A revision of British species of Olynx Förster (Hym., Eulophidae). Entomologist's. Monthly Magazine 1959, 95:49-57.
4. Askew RR. On the biology of inhabitants of oak galls of Cynipidae (Hymenoptera) in Britain. Transactions of the Society for British Entomology 1961, 14:237-268.
5. Askew RR. The biology of the British species of the genus Torymus Dalman (Hymenoptera: Torymidae) associated with galls of Cynipidae (Hymenoptera) on oak, with special reference to alternation of forms. Transactions of the Society for British Entomology 1965, 9:217-232.
6. Askew RR. Hymenoptera 2. Chalcidoidea Section (b). Handbooks for the Identification of British Insects 1968, 1-39.. Vol. 8., Royal Entomological Society of London, London, U.K
7. Askew RR. The diversity of insect communities in leaf-mines and plant galls. Journal of Animal Ecology 1980, 49:817-829.
8. Askew RR. The biology of gall wasps. Biology of Gall Insects 1984, 223-271.. Ananthakrishnan T N. (ed. by., Oxford and IBH Publishing Company, Delhi, India
9. Askew RR, Shaw MR. An account of the Chalcidoidea (Hymenoptera) parasitizing leaf-mining insects of deciduous trees in Britain. Biological Journal of the Linnean Society 1974, 6:289-335.
10. Bailey R, Schönrogge K, Cook JM, Melika G, Csóka G, Thúroczy C. Host niches and defensive extended phenotypes structure parasitoid wasp communities. PLoS Biology 2009, 7:e1000179..
11. Banašek-Richter C, Bersier LF, Cattin MF, Baltensberger R, Gabriel JP, Merz Y. Complexity in quantitative food webs. Ecology 2009, 90:1470-1477.
12. Bersier LF, Banašek-Richter C, Cattin MF. Quantitative descriptors of food-web matrices. Ecology 2002, 83:2394-407.
13. Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K. Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution 2007, 22:148-155.
14. Bouček Z. A study of Central European Eulophidae, I: Eulophinae (Hymenoptera). Sborník Entomologického Oddeleni Národního Musea v Praze 1959a, 33:117-170.
15. Bouček Z. A study of Central European Eulophidae, II: Diaulinopsis and Cirrospilus (Hymenoptera). Sborník Entomologického Oddeleni Národního Musea v Praze 1959b, 33:171-194.
16. Bouček Z. Studies of European Eulophidae, IV: Pediobius Walk. and two allied genera (Hymenoptera). Sborník Entomologického Oddeleni Národního Musea v Praze 1965, 36:5-90.
17. Bouček Z. On some British Megastigmus (Hym. Torymidae), with a revised key to the west European species. Entomologist's Gazette 1970, 21:265-275.
18. Bryan G. The British species of Achrysocharoides (Hymenoptera, Eulophidae). Systematic Entomology 1980, 5:245-262.
19. Bridge PD, Roberts PJ, Spooner BM, Panchal G. On the reliability of published DNA sequences. New Phytologist 2003, 160:43-48.
20. Bukovinszky T, van Veen FJF, Jongema Y, Dicke M. Direct and indirect effects of resource quality on food web structure. Science 2008, 319:804-807.
21. Campbell BC, Steffen-Campbell JD, Werren JH. Phylogeny of the Nasonia species complex (Hymenoptera: Pteromalidae): inferred from an internal transcribed spacer (ITS2) and 28S rDNA sequences. Insect Molecular Biology 1993, 2:225-237.
22. Challis RJ, Mutun S, Nieves-Aldrey J-L, Preuss S, Rokas A, Aebi A. Longitudinal range expansion and cryptic eastern species in the western Palaearctic oak gallwasp Andricus coriarius. Molecular Ecology 2007, 16:2103-2114.
23. Csóka G, Stone GN, Melika G. Biology, ecology and evolution of gall-inducing Cynipinae. Biology, Ecology and Evolution of Gall-inducing Arthropods 2005, 573-642.. Raman A, Schaefer C W, Withers T M. (ed. by., Science Publishers Inc. Enfield, New Hampshire
24. Dormann CF, Fründ J, Blüthgen N, Gruber B. Indices, graphs and null models: analyzing bipartite ecological networks. Open Journal of Ecology 2009, 2:7-24.
25. Dormann CF, Gruber B, Fründ J. Introducing the bipartite package: analysing ecological networks. R News 2008, 8:8-11.
26. Dyer LA, Singer MS, Lill JT, Stireman JO, Gentry GL, Marquis RJ. Host specificity of Lepidoptera in tropical and temperate forests. Nature 2007, 448:696-699.
27. Feeny P. Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 1970, 51:565-581.
28. Floyd R, Abebe E, Papert A, Blaxter M. Molecular barcodes for soil nematode identification. Molecular Ecology 2002, 11:839-850.
29. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 1994, 3:294-299.
30. Funk DJ, Omland KE. Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology, Evolution and Systematics 2003, 34:397-423.
31. Godfray HCJ, Lewis OT, Memmott J. Studying insect diversity in the tropics. Philosophical Transactions of the Royal Society of London B 1999, 354:1811-1824.
32. Govaerts R, Frodin DG. World Checklist and Bibliography of Fagales. 1998, Royal Botanic Gardens, Kew, U.K
33. Graham MWR de V. A Reclassification of the European Tetrastichinae (Hymenoptera: Eulophidae), with a Revision of Certain Genera: Entomology Series 1987, Vol. 55, Bulletin of the British Museum (Natural History), Oxford, U.K
34. Grobler BC, Lewis OT. Response of native parasitoids to a range-expanding host. Ecological Entomology 2008, 33:453-463.
35. Gross T, Rudolf L, Levin SA, Dieckmann U. Generalized models reveal stabilizing factors in food webs. Science 2009, 325:747-750.
36. Hajibabei M, Singer GAC, Hebert PDN, Hickey DA. DNA barcoding: how it complements taxonomy, molecular phylogenetics and population genetics. Trends in Genetics 2007, 23:167-172.
37. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 1999, 41:95-98.
38. Hansson C. Taxonomy and biology of the Palaearctic species of Chrysocharis Förster, 1856 (Hymenoptera: Eulophidae). Entomologica Scandinavica 1985, 26(Suppl.):1-130.
39. Hawkins BA, Cornell HW, Hochberg ME. Predators, parasitoids and pathogens as mortality agents in phytophagous insect populations. Ecology 1997, 78:2145-2152.
40. Hayward A, Stone GN. Comparative phylogeography across two trophic levels: the oak gall wasp Andricus kollari and its chalcid parasitoid Megastigmus stigmatizans. Molecular Ecology 2006, 15:479-489.
41. Heath J, Emmet AM. The Moths and Butterflies of Great Britain and Ireland, Micropterigidae - Heliozelidae 1976, Vol. 1., Blackwell/Curwen, London, U.K
42. Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States America 2004, 101:14812-14817.
43. Hellén W. Zur Kenntnis der phytophagen Cynipiden Finnlands (Hym.). Notulae Entomologicae 1937, 17:31-38.
44. Henneman ML, Memmott J. Infiltration of a Hawaiian community by introduced biological control agents. Science 2001, 293:1314-1316.
45. Henson KSE, Craze PG, Memmott J. The restoration of parasites, parasitoids, and pathogens to heathland communities. Ecology 2009, 90:1840-1851.
46. Heraty J, Hawks D, Kostecki JS, Carmichael A. Phylogeny and behaviour of the Gollumiellinae, a new subfamily of the ant-parasitic Eucharitidae (Hymenoptera: Chalcidoidea). Systematic Entomology 2004, 29:544-559.
47. Heraty JM, Woolley JB, Hopper KR, Hawks DL, Kim J-W, Buffington M. Molecular phylogenetics and reproductive incompatibility in a complex of cryptic species of aphid parasitoids. Molecular Phylogenetics and Evolution 2007, 45:480-493.
48. Hering EM. Bestimmungstabellen der Blattminen von Europa Einschließlich des Mittelmeerbeckens und der Kanarischen Inseln 1957, Vols I-III., Dr W. Junk, 'S-Gravenhage Kluwer Academic, The Hague, The Netherlands.
49. Holt RD. Predation, apparent competition, and the structure of prey communities. Theoretical Population Biology 1977, 12:197-229.
50. Holt RD, Lawton JH. The ecological consequences of shared natural enemies. Annual Review of Ecology and Systematics 1994, 25:495-520.
51. Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Biometrics 2001, 17:754-755.
52. Hurst GDD, Jiggins FM. Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proceedings of the Royal Society of London, Series B 2005, 272:1525-1534.
53. Kankare M, Stefanescu C, van Nouhuys S, Shaw MR. Host specialization by Cotesia wasps (Hymenoptera: Braconidae) parasitizing species-rich Melitaeini (Lepidoptera: Nymphalidae) communities in north-eastern Spain. Biological Journal of the Linnean Society 2005, 86:45-65.
54. King RA, Read DS, Traugott M, Symondson WOC. Molecular analysis of predation: a review of best practice for DNA-based approaches. Molecular Ecology 2008, 17:947-963.
55. Kitching R. Those d... elusive food webs. Trends in Ecology & Evolution 2004, 19:294-295.
56. Knowles LL, Carstens BC. Delimiting species without monophyletic gene trees. Systematic Biology 2007, 56:887-895.
57. Lewis OT, Memmott J, LaSalle J, Lyal CHC, Whitefoord C, Godfray HCF. Structure of a diverse tropical forest insect-parasitoid community. Journal of Animal Ecology 2002, 71:855-873.
58. Liljeblad J, Ronquist F. A phylogenetic analysis of higher-level gall wasp relationships (Hymenoptera: Cynipidae). Systematic Entomology 1998, 23:229-252.
59. Lohse K. Can mtDNA barcodes be used to delimit species? A response to Pons et al. (2006). Systematic Biology 2009, 58:439-442.
60. Macfadyen S, Gibson R, Polaszek A, Morris RJ, Craze PG, Planqué R. Do differences in food web structure between organic and conventional farms affect the ecosystem service of pest control? Ecology Letters 2009, 12:229-238.
61. Marsteller S, Adams DC, Collyer ML, Condon M. Six cryptic species on a single species of host plant: morphometric evidence for possible reproductive character displacement. Ecological Entomology 2009, 34:66-73.
62. May R. Food web assembly and collapse: mathematical models and implications for conservation. Philosophical Transactions of the Royal Society B 2009, 364:1643-1646.
63. Mayer G. Die Einmiethler der mitteleuropäischen Eichengallen. Verhandlung der Zoologisch-Botanischen Geselschaft in Wien 1872, 22:669-726.
64. Memmott J, Godfray HCJ. The use and construction of parasitoid webs. Parasitoid Community Ecology 1994, 300-318.. Hawkins B A, Sheehan W. (ed. by., Oxford University Press, Oxford, U.K
65. Memmott J, Godfray HCJ, Gauld ID. The structure of a tropical host-parasitoid community. Journal of Animal Ecology 1994, 63:521-540.
66. Müller CB, Adriaanse ICT, Belshaw R, Godfray HCJ. The structure of aphid-parasitoid community. Journal of Animal Ecology 1999, 68:346-370.
67. Nicholls JA, Preuss S, Hayward A, Melika G, Čsoka G, Nieves-Aldrey JL. Concordant phylogeography and cryptic speciation in two Western Palaearctic oak gall parasitoid species complexes. Molecular Ecology 2010, 19:592-609.
68. Nieves-Aldrey JL. Hymenoptera, Cynipidae. Fauna Iberica 2001, Ramos M A. Vol. 16 (ed. by, J. A. ercedor, X. B. Ros, J. G. Noguera, A. G. Sierra, and, E. M. Mayol, Museo Nacional de Ciencias Naturales, Madrid, Spain
69. Novotny V, Basset Y, Miller SE, Weiblen GD, Bremer B, Cizek L. Low host specificity of herbivorous insects in a tropical forest. Nature 2002, 416:841-844.
70. Noyes JS. Interactive catalogue of World Chalcidoidea 2001. Taxapad - Scientific Names for Information Management. 2002, Taxapod and The Natural History Museum, Vancouver, Canada
71. Paniagua MR, Medianero E, Lewis OT. Structure and vertical stratification of plant galler-parasitoid food webs in two tropical forests. Ecological Entomology 2009, 34:310-320.
72. Parker SR. Sequence Navigator. Multiple sequence alignment software. Methods in Molecular Biology 1997, 70:145-154.
73. Penzes Z, Melika G, Bozsóki G, Bihari P, Mikó I, Tavakoli M. Systematic re-appraisal of the gall-usurping wasp genus Synophrus Hartig, 1843 (Hymenoptera: Cynipidae: Synergini). Systematic Entomology 2009, 34:688-711.
74. Pfenninger M, Schwenk K. Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evolutionary Biology 2007, 7:121..
75. Pfenninger M, Nowak C, Kley C, Steinke D, Streit B. Utility of DNA taxonomy and barcoding for the inference of larval community structure in morphologically cryptic Chironomus (Diptera) species. Molecular Ecology 2007, 16:1957-1968.
76. Posada D. jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution 2008, 25:1253-1256.
77. Pujade-Villar J, Melika G, Ros-Farré P, Ács Z, Csóka G. Cynipid inquiline wasps of Hungary, with taxonomic notes on the Western Palaearctic fauna (Hymenoptera: Cynipidae, Cynipinae, Synergini). Folia Entomologica Hungarica 2003, 64:121-170.
78. Quicke DLJ. The world of DNA bar-coding and morphology - collision or synergism and what of the future? The Systematist 2004, 23:8-12.
79. Ronquist F. Evolution of parasitism among closely related species: phylogenetic relationships and the origin of inquilinism in gall wasps (Hymenoptera, Cynipidae). Evolution 1994, 48:241-266.
80. Rosenberg NA. Statistical tests for taxonomic distinctiveness from observations of monophyly. Evolution 2007, 61:317-323.
81. Schönrogge K, Crawley MJ. Quantitative webs as a means of assessing the impact of alien insects. Journal of Animal Ecology 2000, 69:841-868.
82. Schönrogge K, Stone GN, Crawley MJ. Spatial and temporal variation in guild structure: Parasitoids and Inquilines of Andricus quercuscalicis Burgsd. (Hymenoptera: Cynipidae) in its native and alien ranges. Oikos 1995, 72:51-60.
83. Schönrogge K, Stone GN, Crawley MJ. Alien herbivores and native parasitoids: rapid development of guild structure in an invading gall wasp, Andricus quercuscalicis (Hymenoptera: Cynipidae). Ecological Entomology 1996a, 21:71-80.
84. Schönrogge K, Stone GN, Crawley MJ. Abundance patterns and species richness of the parasitoids and inquilines of the alien gall former Andricus quercuscalicis Burgsdorf (Hymenoptera: Cynipidae). Oikos 1996b, 77:507-518.
85. Sha Z-L, Zhu CD, Murphy RW, Huang D-W. Diglyphus isaea (Hymenoptera: Eulophidae): a probable complex of cryptic species that forms an important biological control agent of agromyzid leaf miners. Journal of Zoological Systematics and Evolutionary Research 2006a, 45:128-135.
86. Sha Z-L, Zhu CD, Murphy RW, LaSalle J, Huang D-W. Mitochondrial phylogeography of a leafminer parasitoid, Diglyphus isaea (Hymenoptera: Eulophidae) in China. Biological Control 2006b, 38:380-389.
87. Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 1994, 87:651-701.
88. Smith MA, Woodley NE, Janzen DH, Hallwachs W, Hebert PDN. DNA barcodes reveal cryptic host-specificity within the presumed polyphagous members of a genus of parasitoid flies (Diptera: Tachinidae). Proceedings of the National Academy of Sciences of the United States of America 2006, 103:3657-3662.
89. Smith MA, Rodriguez JJ, Whitfield JB, Deans AR, Janzen DH, Hallwachs W. Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:12359-12364.
90. Southwood TRE. The number of species of insects associated with various trees. Journal of Animal Ecology 1961, 30:1-8.
91. Stone GN, Atkinson RJ, Rokas A, Csóka G, Nieves-Aldrey J-L. Differential success in northwards range expansion between ecotypes of the marble gallwasp Andricus kollari. Molecular Ecology 2001, 10:761-778. the tale of two lifecycles.
92. Stone GN, Hernandez-Lopez A, Nicholls JA, di Pierro E, Pujade-Villar J, Melika G. Extreme host plant conservatism during at least 20 million years of host plant pursuit by oak gallwasps. Evolution 2009, 63:854-869.
93. Traugott M, Bell JR, Broad GR, Powell W, van Veen FJF, Vollhart IMG. Endoparasitism in cereal aphids: molecular analysis of a whole parasitoid community. Molecular Ecology 2008, 17:3928-3938.
94. Tylianakis JM, Tscharntke T, Lewis OT. Habitat modification alters the structure of tropical host-parasitoid food webs. Nature 2007, 445:202-205.
95. Valladares GR, Salvo A, Godfray HCJ. Quantitative food webs of dipteran leafminers and their parasitoids in Argentina. Ecological Research 2001, 16:925-939.
96. van Veen FJF, Belshaw R, Godfray HCJ. The value of the ITS2 region for the identification of species boundaries between Alloxysta hyperparasitoids (Hymenoptera: Charipidae) of aphids. European Journal of Entomology 2003, 100:449-453.
97. van Veen FJF, Morris RJ, Godfray HCJ. Apparent competition, quantitative food webs, and the structure of phytophagous insect communities. Annual Review of Entomology 2006, 51:187-208.
98. Wiebes-Rijks AA. A character analysis of the species of Synergus Hartig, Section II (Mayer, 1872) (Hymenoptera, Cynipidae). Zoologische Mededeelingen 1979, 53:297-321.