BIN overlap confirms transcontinental distribution of pest aphids (Hemiptera: Aphididae)

Autoři: Muhammad Tayyib Naseem aff001;  Muhammad Ashfaq aff003;  Arif Muhammad Khan aff001;  Akhtar Rasool aff001;  Muhammad Asif aff001;  Paul D. N. Hebert aff003
Působiště autorů: National Institute for Biotechnology and Genetic Engineering, Faisalabad, Pakistan aff001;  Pakistan Institute of Engineering and Applied Sciences, Islamabad, Pakistan aff002;  Centre for Biodiversity Genomics & Department of Integrative Biology, University of Guelph, Guelph, ON, Canada aff003;  Department of Biotechnology, University of Sargodha, Sargodha, Pakistan aff004;  Department of Zoology, University of Swat, Swat, Pakistan aff005
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article


DNA barcoding is highly effective for identifying specimens once a reference sequence library is available for the species assemblage targeted for analysis. Despite the great need for an improved capacity to identify the insect pests of crops, the use of DNA barcoding is constrained by the lack of a well-parameterized reference library. The current study begins to address this limitation by developing a DNA barcode reference library for the pest aphids of Pakistan. It also examines the affinities of these species with conspecific populations from other geographic regions based on both conventional taxonomy and Barcode Index Numbers (BINs). A total of 809 aphids were collected from a range of plant species at sites across Pakistan. Morphological study and DNA barcoding allowed 774 specimens to be identified to one of 42 species while the others were placed to a genus or subfamily. Sequences obtained from these specimens were assigned to 52 BINs whose monophyly were supported by neighbor-joining (NJ) clustering and Bayesian inference. The 42 species were assigned to 41 BINs with 38 showing BIN concordance. These species were represented on BOLD by 7,870 records from 69 countries. Combining these records with those from Pakistan produced 60 BINs with 12 species showing a BIN split and three a BIN merger. Geo-distance correlations showed that intraspecific divergence values for 49% of the species were not affected by the distance between populations. Forty four of the 52 BINs from Pakistan had counterparts in 73 countries across six continents, documenting the broad distributions of pest aphids.

Klíčová slova:

Aphids – Cryptic speciation – DNA barcoding – DNA libraries – DNA sequence analysis – Insect pests – Pakistan – Sequence analysis


1. Braendle C, Davis GK, Brisson JA, Stern DL. Wing dimorphism in aphids. Heredity. 2006;97: 192. doi: 10.1038/sj.hdy.6800863 16823401

2. Ogawa K, Miura T. Aphid polyphenisms: trans-generational developmental regulation through viviparity. Front Physiol. 2014;5: 1. doi: 10.3389/fphys.2014.00001 24478714

3. Favret C. Aphid species file version 5.0/5.0 [2019.02].

4. Blackman R, Eastop V. Aphids on the world’s plants: An online identification and information guide; 2014.

5. Blackman RL, Eastop VF. Taxonomic issues. In: Emden H F van, Harrington R, editors. Aphids as crop pests: CAB International; 2007. pp. 1–27.

6. Dixon AFG, Kindlmann P, Leps J, Holman J. Why there are so few species of aphids especially in the tropics. Am Nat. 1987;129: 580–592.

7. Sewell GH, Storch RH, Manzer FE, Forsythe HY Jr. The relationship between coccinellids and aphids in the spread of potato leafroll virus in a greenhouse. Am J Potato Res. 1990;67: 865–868.

8. Mosco MC, Arduino P, Bullini L, Barbagallo S. Genetic heterogeneity, reproductive isolation and host preferences in mealy aphids of the Hyalopterus pruni complex (Homoptera, Aphidoidea). Mol. Ecol. 1997;6: 667–670.

9. Carletto J, Blin A, Vanlerberghe-Masutti F. DNA-based discrimination between the sibling species Aphis gossypii Glover and Aphis frangulae Kaltenbach. Syst Entomol. 2009;34: 307–314.

10. Sorensen JT. Aphids In: Cardé RT, Resh VH, editors. Encyclopedia of insects, 2nd edition. San Diego, USA: Academic Press; 2009. p. 27–31.

11. Raymond B, Searle JB, Douglas AE. On the processes shaping reproductive isolation in aphids of the Aphis fabae (scop.) complex (Aphididae: Homoptera). Biol J Linnean Soc. 2001;74: 205–215.

12. Brisson JA. Aphid wing dimorphisms: linking environmental and genetic control of trait variation. Philosophical Transactions of the Royal Society of London Series B, Biol Sci. 2010;365(1540): 605–16.

13. Jayaseelan M, Roesler Uwe R. MALDI-TOF MS Profiling-Advances in species identification of pests, parasites, and vectors. Front Cell Infect Microbiol. 2017;7: 184. doi: 10.3389/fcimb.2017.00184 28555175

14. Naaum AM, Foottit RG, Maw HEL, Hanner R. Real-time PCR for identification of the soybean aphid, Aphis glycines Matsumura. J Appl Entomol. 2014;138: 485–9.

15. Kinyanjui G, Khamis FM, Mohamed S, Ombura LO, Warigia M, Ekesi S. Identification of aphid (Hemiptera: Aphididae) species of economic importance in Kenya using DNA barcodes and PCR-RFLP-based approach. Bull Entomol Res. 2016;106: 63–72. doi: 10.1017/S0007485315000796 26490301

16. Nunez JCB, Oleksiak MF. A cost-effective approach to sequence hundreds of complete mitochondrial genomes. PLOS ONE. 2016;11: e0160958. doi: 10.1371/journal.pone.0160958 27505419

17. Caterino MS, Cho S, Sperling FA. The current state of insect molecular systematics: A thriving Tower of Babel. Annu Rev Entomol. 2000;45: 1–54. doi: 10.1146/annurev.ento.45.1.1 10761569

18. Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, et al. Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol. 2006;55: 595–609. doi: 10.1080/10635150600852011 16967577

19. Erlandson M, Braun L, Baldwin D, Soroka J, Ashfaq M, Hegedus D. Molecular markers for Peristenus spp. (Hymenoptera: Braconidae) parasitoids associated with Lygus spp. (Hemiptera: Miridae). Can Entomol. 2003;135: 71–83.

20. Ashfaq M, Ara J, Noor AR, Hebert PDN, Mansoor S. Molecular phylogenetic analysis of a scale insect (Drosicha mangiferae; Hemiptera: Monophlebidae) infesting mango orchards in Pakistan. Eur J Entomol. 2011;108: 553–559.

21. Chen R, Jiang L-Y, Qiao G-X. The effectiveness of three regions in mitochondrial genome for aphid DNA barcoding: A case in Lachininae. PLOS ONE. 2012;7: e46190. doi: 10.1371/journal.pone.0046190 23056258

22. Ashfaq M, Noor AR, Mansoor S. DNA-based characterization of an invasive mealybug (Hemiptera: Pseudococcidae) species damaging cotton in Pakistan. Appl Entomol Zool. 2010;45: 395–404.

23. Liu J, Jiang J, Song S, Tornabene L, Chabarria R, Naylor GJP, et al. Multilocus DNA barcoding–species identification with multilocus data. Sci Rep. 2017;7: 16601. doi: 10.1038/s41598-017-16920-2 29192249

24. Hebert PDN, Cywinska A, Ball SL. Biological identifications through DNA barcodes. Proceedings of the Royal Society of London B: Biol Sci. 2003;270: 313–321.

25. Hebert PDN, Ratnasingham S, de Waard JR. Barcoding animal life: Cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London B: Biol Sci. 2003;270(Suppl 1): S96–S99.

26. Ander M, Troell K, Chirico J. Barcoding of biting midges in the genus Culicoides: a tool for species determination. Med Vet Entomol. 2013;27: 323–31. doi: 10.1111/j.1365-2915.2012.01050.x 23106166

27. Adams M, Raadik TA, Burridge CP, Georges A. Global biodiversity assessment and hyper-cryptic species complexes: more than one species of elephant in the room? Syst Biol. 2014;63: 518–33. doi: 10.1093/sysbio/syu017 24627185

28. Iftikhar R, Ashfaq M, Rasool A, Hebert PDN. DNA barcode analysis of thrips (Thysanoptera) diversity in Pakistan reveals cryptic species complexes. PLOS ONE. 2016;11: e0146014. doi: 10.1371/journal.pone.0146014 26741134

29. Foottit RG, Maw HEL, Von Dohlen CD, Hebert PDN. Species identification of aphids (Insecta: Hemiptera: Aphididae) through DNA barcodes. Mol Ecol Resour. 2008;8: 1189–1201. doi: 10.1111/j.1755-0998.2008.02297.x 21586006

30. Liu Q-H, Jiang L-Y, Qiao G-X. DNA barcoding of Greenideinae (Hemiptera: Aphididae) with resolving taxonomy problems. Invertebr Syst. 2013;27: 428–438.

31. Cocuzza GE, Cavalieri V. Identification of aphids of Aphis frangulae-group living on Lamiaceae species through DNA barcode. Mol Ecol Resour. 2014;14: 447–57. doi: 10.1111/1755-0998.12199 24188728

32. Gwiazdowski RA, Foottit RG, Maw HEL, Hebert PDN. The Hemiptera (Insecta) of Canada: constructing a reference library of DNA barcodes. PLOS ONE. 2015;10: e0125635. doi: 10.1371/journal.pone.0125635 25923328

33. Sow A, Brévault T, Benoit L, Chapuis M-P, Galan M, Coeur d’acier A, et al. Deciphering host-parasitoid interactions and parasitism rates of crop pests using DNA metabarcoding. Sci Rep. 2019;9: 3646. doi: 10.1038/s41598-019-40243-z 30842584

34. Piper AM, Batovska J, Cogan NOI, Weiss J, Cunningham JP, Rodoni BC, et al. Prospects and challenges of implementing DNA metabarcoding for high-throughput insect surveillance. GigaScience. 2019;8: 1–22.

35. Ritter CD, Häggqvist S, Karlsson D, Sääksjärvi IE, Muasya AM, Nilsson RH, et al. Biodiversity assessments in the 21st century: the potential of insect traps to complement environmental samples for estimating eukaryotic and prokaryotic diversity using high-throughput DNA metabarcoding. Genome. 2019;62: 147–159. doi: 10.1139/gen-2018-0096 30673361

36. Galimberti A, Ferri E, De Mattia F, Labra M, Casiraghi M. DNA barcoding: a six-question tour to improve users' awareness about the method. Brief Bioinform. 2010;11: 440–53. doi: 10.1093/bib/bbq003 20156987

37. Ratnasingham S, Hebert PDN. BOLD: The Barcode of Life Data System ( Mol Ecol Notes. 2007;7: 355–364. doi: 10.1111/j.1471-8286.2007.01678.x 18784790

38. Ratnasingham S, Hebert PDN. A DNA-based registry for all animal species: The Barcode Index Number (BIN) system. PLOS ONE. 2013;8: e66213. doi: 10.1371/journal.pone.0066213 23861743

39. Mutanen M, Kekkonen M, Prosser SWJ, Hebert PDN, Kaila L. One species in eight: DNA barcodes from type specimens resolve a taxonomic quagmire. Mol Ecol Resour. 2015;15: 967–984. doi: 10.1111/1755-0998.12361 25524367

40. Ortiz AS, Rubio RM, Guerrero JJ, Garre MJ, Serrano J, Hebert PDN, et al. Close congruence between Barcode Index Numbers (BINs) and species boundaries in the Erebidae (Lepidoptera: Noctuoidea) of the Iberian Peninsula. Biodivers data J. 2017;5: e19840.

41. Hebert PDN, Ratnasingham S, Zakharov EV, Telfer AC, Levesque-Beaudin V, Milton MA, et al. Counting animal species with DNA barcodes: Canadian insects. Phil Trans R Soc Lond B: Biol Sci. 2016;371: 1702.

42. Lee Y, Lee W, Kanturski M, Foottit RG, Akimoto SI, Lee S. Cryptic diversity of the subfamily Calaphidinae (Hemiptera: Aphididae) revealed by comprehensive DNA barcoding. PLOS ONE. 2017;12: e0176582. doi: 10.1371/journal.pone.0176582 28448639

43. Ashfaq M, Sabir JSM, El-Ansary HO, Perez K, Levesque-Beaudin V, Khan AM, et al. Insect diversity in the Saharo-Arabian region: Revealing a little-studied fauna by DNA barcoding. PLOS ONE. 2018;13: e0199965. doi: 10.1371/journal.pone.0199965 29985924

44. deWaard JR, Mitchell A, Keena MA, Gopurenko D, Boykin LM, Armstrong KF, et al. Towards a global barcode library for Lymantria (Lepidoptera: Lymantriinae) tussock moths of biosecurity concern. PLOS ONE. 2010;5: e14280. doi: 10.1371/journal.pone.0014280 21151562

45. Virgilio M, Jordaens K, Breman FC, Backeljau T, De Meyer M. Identifying insects with incomplete DNA barcode libraries, African fruit flies (Diptera: Tephritidae) as a test case. PLOS ONE. 2012;7: e31581. doi: 10.1371/journal.pone.0031581 22359600

46. Coeur d'Acier A, Cruaud A, Artige E, Genson G, Clamens AL, Pierre E, et al. DNA barcoding and the associated phylaphidb@se website for the identification of European aphids (Insecta: Hemiptera: Aphididae). PLOS ONE. 2014;9: e97620. doi: 10.1371/journal.pone.0097620 24896814

47. Ashfaq M, Akhtar S, Khan AM, Adamowicz SJ, Hebert PDN. DNA barcode analysis of butterfly species from Pakistan points towards regional endemism. Mol Ecol Resour. 2013;13(5):832–843. doi: 10.1111/1755-0998.12131 23789612

48. Raupach MJ, Hannig K, Moriniere J, Hendrich L. A DNA barcode library for ground beetles of Germany: the genus Amara Bonelli, 1810 (Insecta, Coleoptera, Carabidae). Zookeys. 2018;759: 57–80.

49. Cho SY, Suh KI, Bae YJ. DNA barcode library and its efficacy for identifying food‐associated insect pests in Korea. Entomol Res. 2013;43: 253–261.

50. Ashfaq M, Hebert PDN. DNA barcodes for bio-surveillance: Regulated and economically important arthropod plant pests. Genome 2016;59: 933–945. doi: 10.1139/gen-2016-0024 27753511

51. Kirichenko NI, Petkoa VM, Magnoux CE, Lopez-Vaamonde C. Diversity and distribution of leaf mining insects on birches (Betula spp.) in Siberia. Entomol Rev. 2017;97: 183–197.

52. Ren J-M, Ashfaq M, Hu X-N, Ma J, Liang F, Hebert PDN, et al. Barcode Index Numbers expedite quarantine inspections and aid the interception of nonindigenous mealybugs (Pseudococcidae). Biol Invasions 2018;20: 449–460.

53. Foottit RG, Maw HEL, Pike KS. DNA barcodes to explore diversity in aphids (Hemiptera: Aphididae and Adelgidae). Redia 2009;92: 87–91.

54. Lee W, Kim H, Lim J, Choi HR, Kim Y, Kim YS, et al. Barcoding aphids (Hemiptera: Aphididae) of the Korean Peninsula: Updating the global data set. Mol Ecol Resour. 2011;11: 32–37. doi: 10.1111/j.1755-0998.2010.02877.x 21429098

55. Blackman RL, Eastop VF. Aphids on the world’s crop: An identification and information guide, 2nd Edition. Wiley; 2000.

56. Martin JH. The identification of common aphid pests of tropical agriculture. Trop Pest Manag. 1983;29: 395–411.

57. Ivanova NV, deWaard JR, Hebert PDN. An inexpensive, automation-friendly protocol for recovering high quality DNA. Mol Ecol Notes 2006;6: 998–1002.

58. Porco D, Rougerie R, Deharveng L, Hebert P. Coupling non‐destructive DNA extraction and voucher retrieval for small soft‐bodied arthropods in a high‐throughput context: The example of Collembola. Mol Ecol Resour. 2010;10: 942–945. doi: 10.1111/j.1755-0998.2010.2839.x 21565103

59. Hebert PDN, Dewaard JR, Zakharov EV, Prosser SW, Sones JE, McKeown JT, et al. A DNA 'barcode blitz': rapid digitization and sequencing of a natural history collection. PLOS ONE. 2013;8: e68535. doi: 10.1371/journal.pone.0068535 23874660

60. Park DS, Foottit R, Maw E, Hebert PDN. Barcoding bugs: DNA-based identification of the true bugs (Insecta: Hemiptera: Heteroptera). PLOS ONE. 2011;6: e18749. doi: 10.1371/journal.pone.0018749 21526211

61. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30: 2725–2729. doi: 10.1093/molbev/mst197 24132122

62. Meyer CP, Paulay G. DNA barcoding: Error rates based on comprehensive sampling. PLOS BIOL. 2005;3: e422. doi: 10.1371/journal.pbio.0030422 16336051

63. Thompson JD, Higgins DG, Gibson TJ. Clustal W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22: 4673–4680. doi: 10.1093/nar/22.22.4673 7984417

64. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980;16: 111–120. doi: 10.1007/bf01731581 7463489

65. Felsenstein J. Confidence limits on phylogenies: An approach using the bootstrap. Evolution. 1985;39: 783–791. doi: 10.1111/j.1558-5646.1985.tb00420.x 28561359

66. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, et al. Mrbayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61: 539–542. doi: 10.1093/sysbio/sys029 22357727

67. Librado P, Rozas J. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009;25: 1451–1452. doi: 10.1093/bioinformatics/btp187 19346325

68. Mantel N. The detection of disease clustering and a generalized regression approach. Cancer Res. 1967;27: 209–220. 6018555

69. Blagoev GA, deWaard JR, Ratnasingham S, deWaard SL, Lu L, Robertson J, et al. Untangling taxonomy: a DNA barcode reference library for Canadian spiders. Mol Ecol Resour. 2016;16: 325–341. doi: 10.1111/1755-0998.12444 26175299

70. Naumann-Etienne K, Remaudiere G. A commented preliminary checklist of the aphids (Homoptera: Aphididae) of Pakistan and their host plants. Parasitica 1995;51: 61.

71. Irshad M. Aphids and their biological control in Pakistan. Pak J Biol Sci. 2001;4: 537–541.

72. Kanturski M, Zia A, Rafi MA. The Lachnus of Pakistan with description of a new species (Hemiptera: Aphididae: Lachninae). J Asia-Pac Entomol. 2017;20: 1219–1227.

73. Bodlah I, Naeem M, Mohsin A. Checklist distribution host range and ecology of Aphidoidea (Homoptera) from the rainfed region of Punjab province of Pakistan, Sarhad J Agric. 2011;27: 93–101.

74. Hamid S. Natural balance of graminicolous aphids in Pakistan. Survey of populations. Agronomie 1983;3: 665–673.

75. Amin M, Mahmood K, Bodlah I. Aphid species (Hemiptera: Aphididae) infesting medicinal and aromatic plants in the Poonch division of Azad Jammu and Kashmir, Pakistan. J Animal Plant Sci. 2017;27: 1377–1385.

76. Scheffer SJ, Lewis ML, Gaimari SD, Reitz SR. Molecular survey for the invasive leafminer pest Liriomyza huidobrensis (Diptera: Agromyzidae) in California uncovers only the native pest Liriomyza langei. J Econ Entomol. 2014;107: 1959–64. doi: 10.1603/EC13279 26309286

77. deWaard JR, Hebert PDN, Humble LM. A comprehensive DNA barcode library for the looper moths (Lepidoptera: Geometridae) of British Columbia, Canada. PLOS ONE. 2011;6: e18290. doi: 10.1371/journal.pone.0018290 21464900

78. Hodgetts J, Ostoja-Starzewski JC, Prior T, Lawson R, Hall J, Boonham N. DNA barcoding for biosecurity: case studies from the UK plant protection program. Genome. 2016;59: 1033–48. doi: 10.1139/gen-2016-0010 27792411

79. Ashfaq M, Hebert PDN, Mirza MS, Khan AM, Mansoor S, Shah GS, et al. DNA barcoding of Bemisia tabaci complex (Hemiptera: Aleyrodidae) reveals southerly expansion of the dominant whitefly species on cotton in Pakistan. PLOS ONE. 2014;9: e104485. doi: 10.1371/journal.pone.0104485 25099936

80. Lagos-Kutz D, Favret C, Giordano R, Voegtlin DJ. Molecular and morphological differentiation between Aphis gossypii Glover (Hemiptera, Aphididae) and related species, with particular reference to the North American Midwest. ZooKeys. 2014;459: 49–72.

81. Singh G, Singh NP, Singh R, Singh G, Singh NP. Food plants of a major agricultural pest Aphis gossypii Glover (Homoptera: Aphididae) from India: An updated checklist. Int J Life Sci Biotechnol Pharma Res. 2014;3: 1–26.

82. Wang JF, Qiao GX. DNA barcoding of genus Toxoptera Koch (Hemiptera: Aphididae): Identification and molecular phylogeny inferred from mitochondrial COI sequences. Insect Sci. 2009;16: 475–484.

83. Cocuzza GE, Cavalieri V, Barbagallo S. Preliminary results in the taxonomy of the cryptic group Aphis frangulae/gossypii obtained from mitochondrial DNA sequence. Bull Insectology. 2008;61: 125–126.

84. Janzen DH, Burns JM, Cong Q, Hallwachs W, Dapkey T, Manjunath R, et al. Nuclear genomes distinguish cryptic species suggested by their DNA barcodes and ecology. Proc Natl Acad Sci USA. 2017.

85. 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. Proc Natl Acad Sci USA. 2004;101: 14812–7. doi: 10.1073/pnas.0406166101 15465915

86. Bortolus A. Error cascades in the biological sciences: the unwanted consequences of using bad taxonomy in ecology. Ambio. 2008;37: 114–8. doi: 10.1579/0044-7447(2008)37[114:ecitbs];2 18488554

87. Kang AR, Kim MJ, Park IA, Kim KY, Kim I. Extent and divergence of heteroplasmy of the DNA barcoding region in Anapodisma miramae (Orthoptera: Acrididae). Mitochondrial DNA A. 2016;27: 3405–3414.

88. Weber AA.-T, Stöhr S, Chenuil A. Species delimitation in the presence of strong incomplete lineage sorting and hybridization: Lessons from Ophioderma (Ophiuroidea: Echinodermata). Mol Phylogenet Evol. 2019;131: 138–148. doi: 10.1016/j.ympev.2018.11.014 30468939

89. Peccoud J, Ollivier A, Plantegenest M, Simon J-C. A continuum of genetic divergence from sympatric host races to species in the pea aphid complex. Proc Natl Acad Sci USA. 2009;106: 7495–7500. doi: 10.1073/pnas.0811117106 19380742

90. Virgilio M, Backeljau T, Nevado B, De Meyer M. Comparative performances of DNA barcoding across insect orders. BMC Bioinformatics. 2010;11: 206. doi: 10.1186/1471-2105-11-206 20420717

91. Bergsten J, Bilton DT, Fujisawa T, Elliott M, Monaghan MT, Balke M, et al. The effect of geographical scale of sampling on DNA barcoding. Syst Biol. 2012;61: 851–69. doi: 10.1093/sysbio/sys037 22398121

92. Huemer P, Mutanen M, Sefc KM, Hebert PDN. Testing DNA barcode performance in 1000 species of European Lepidoptera: large geographic distances have small genetic impacts. PLOS ONE. 2014;9: e115774. doi: 10.1371/journal.pone.0115774 25541991

93. Ashfaq M, Akhtar S, Rafi MA, Mansoor S, Hebert PDN. Mapping global biodiversity connections with DNA barcodes: Lepidoptera of Pakistan. PLOS ONE. 2017;12: e0174749. doi: 10.1371/journal.pone.0174749 28339501

94. Ashfaq M, Blagoev G, Tahir HM, Khan AM, Mukhtar MK, Akhtar S, et al. Assembling a DNA barcode reference library for the spiders (Arachnida: Araneae) of Pakistan. PLOS ONE. 2019;14: e0217086. doi: 10.1371/journal.pone.0217086 31116764

95. Irwin ME, Kampmeier GE, Weisser WW. Aphid movement: process and consequences. In: Emden HF, van Harrington R, editors. Aphids as crop pests. 2007; p. 153–186.

96. Harrington R, Verrier P, Denholm C, Hulle M, Maurice D, Bell N, et al. EXAMINE (Exploitation of Aphid Monitoring in Europe): an European thematic network for the study of global change impacts on aphids. In: Simon JC, Dedryver CA, Rispe C, Hulle M, editors. Aphids in a New Millennium. Science Update 2004. p. 45–49.

97. Hull M, Renoust M, Turpeau E. New aphid species detected by permanent aerial sampling programmes in France. In: Nieto Nafria JM, Dixon AEG, editors. Aphids in natural and managed ecosystems. Universidad de Leon, Leon, Spain. 1998. pp. 365–369.

98. Miller GL, Halbert SE, Foottit RG. North American adventive aphids: appraising the faunal components. 7th International Symposium on Aphids, Freemantle Australia. 2005.

Článek vyšel v časopise


2019 Číslo 12
Nejčtenější tento týden