Molecular analysis reveals high compartmentalization in aphid-primary parasitoid networks and low parasitoid sharing between crop and noncrop habitats

Molecular Ecology

Volumn 23, Issue 15, 2014, Pages 3900-3911

  Derocles, Stephane A P ^a,b   Le Ralec, Anne ^a   Besson, Mathilde M ^a   Maret, Marion ^a   Walton, Alan ^a   Evans, Darren M ^b   Plantegenest, Manuel ^a  

^a AGROCAMPUS OUEST   (France)

^b UNIVERSITY OF HULL   (United Kingdom)

Author keywords

16S rRNA; agroecosystems; Aphidiinae parasitoids; apparent competition; food webs; host parasitoid communities

Indexed keywords

APHIDIDAE; APHIDIINAE; HEXAPODA;

RNA 16S;

AGRICULTURE; AGROECOSYSTEMS; ANIMAL; APHID; APHIDIINAE PARASITOIDS; APPARENT COMPETITION; COMPETITIVE BEHAVIOR; CONFERENCE PAPER; CROP; ECOSYSTEM; FOOD CHAIN; FOOD WEBS; FRANCE; HOST-PARASITOID COMMUNITIES; HYMENOPTERA; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PARASITOLOGY;

16S RRNA; AGROECOSYSTEMS; APHIDIINAE PARASITOIDS; APPARENT COMPETITION; FOOD WEBS; HOST-PARASITOID COMMUNITIES;

AGRICULTURE; ANIMALS; APHIDS; COMPETITIVE BEHAVIOR; CROPS, AGRICULTURAL; ECOSYSTEM; FOOD CHAIN; FRANCE; HYMENOPTERA; MOLECULAR SEQUENCE DATA;

EID: 84904745700     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12701     Document Type: Conference Paper

References (74)

1. Alhmedi A, Haubruge E, D'Hoedt S, Francis F, (2011) Quantitative food webs of herbivore and related beneficial community in non-crop and crop habitats. Biological Control, 58, 103-112.
2. Baer CF, Tripp DW, Bjorksten TA, Antolin MF, (2004) Phylogeography of a parasitoid wasp (Diaeretiella rapae): no evidence of host-associated lineages. Molecular Ecology, 13, 1859-1869.
3. Barahoei H, Madjdzadeh SM, Mehrparvar M, (2011) Morphometric differentiation of five biotypes of Lysiphlebus fabarum (Marshall) (Hymenoptera: Braconidae: Aphidiinae) in Iran. Zootaxa, 2745, 43-52.
4. Bersier LF, Banasek-Richter C, Cattin MF, (2002) Quantitative descriptors of food-web matrices. Ecology, 83, 2394-2407.
5. Bilodeau E, Simon JC, Guay JF, Turgeon J, Cloutier C, (2013) Does variation in host plant association and symbiont infection of pea aphid populations induce genetic and behaviour differentiation of its main parasitoid, Aphidius ervi? Evolutionary Ecology, 27, 165-184.
6. Blackman RL, Eastop VF, (1994) Aphids on the World's Trees. An Identification and Information Guide. CABI, Wallingford, Oxon, UK.
7. Blackman RL, Eastop VF, (2000) Aphids on the World's Crops, An Identification and Information Guide, 2nd edn. John Wiley & Sons, Chichester, UK.
8. Blackman RL, Eastop VF, (2006) Aphids on the World's Herbaceous Plants and Shrubs.Volume 2: The Aphids. John Wiley & Sons, Chichester, UK.
9. Blamey M, Grey-Wilson C, (2003) The Illustrated Flora of Britain and Northern Europe. Domino Books, UK.
10. Bonsall MB, Hassell MP, (1998) Apparent competition structures ecological assemblages. Nature, 388, 371-373.
11. Bridge PD, Roberts PJ, Spooner BM, Panchal G, (2003) On the reliability of published DNA sequences. New Phytologist, 160, 43-48.
12. Bukovinszky T, van Veen FJF, Jongema Y, Marcel Dicke M, (2008) Direct and indirect effects of resource quality on food web structure. Science, 319, 804-807.
13. Chacoff NP, Vázquez DP, Lomáscolo SB, Stevani EL, Dorado J, Padrõn B, (2012) Evaluating sampling completeness in a desert plant-pollinator network. Journal of Animal Ecology, 81, 190-200.
14. Chao A, (2005) Species estimation and applications. In: Encyclopedia of Statistical Sciences (eds, Balakrishnan N, Read CB, Vidakovic B,), pp. 7907-7916. Wiley, New York.
15. Derocles SAP, Plantegenest M, Simon JC, Taberlet P, Le Ralec A, (2012a) A universal method for the detection and the identification of Aphidiinae parasitoids within their aphid hosts. Molecular Ecology Resources, 12, 634-645.
16. Derocles SAP, Le Ralec A, Plantegenest M, et al,. (2012b) Identification of molecular markers for DNA barcoding in the Aphidiinae (Hym. Braconidae). Molecular Ecology Resources, 12, 197-208.
17. Elzinga JA, van Nouhuys S, van Leeuwen DJ, Biere A, (2007) Distribution and colonisation ability of three parasitoids and their herbivorous host in a fragmented landscape. Basic and Applied Ecology, 8, 75-88.
18. English-Loeb GM, Brody AK, Karban R, (1993) Host plant-mediated interactions between a generalist folivore and its tachinid parasitoid. Journal of Animal Ecology, 62, 465-471.
19. Evans DM, Pocock MJO, Memmott J, (2013) The robustness of a network of ecological networks to habitat loss. Ecological letters, 16, 844-852.
20. Gardenfors U, (1986) Taxonomic and biological revision of Palearctic Ephedrus Haliday (Hymenoptera: Braconidae, Aphidiinae). Entomologica Scandinavica, 27, 95.
21. Gariepy TD, Messing RH, (2012) Development and use of molecular diagnostic tools to determine trophic links and interspecific interactions in aphid-parasitoid communities in Hawaii. Biological Control, 60, 26-38.
22. Gariepy TD, Kuhlmann U, Gillott C, Erlandson M, (2008) A largescale comparison of conventional and molecular methods for the evaluation of host-parasitoid associations in non-target risk-assessment studies. Journal of Applied Ecology, 15, 481-495.
23. Gotelli NJ, Colwell RK, (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters, 4, 379-391.
24. Greenstone MH, (2006) Molecular methods for assessing insect parasitism. Bulletin of Entomological Research, 96, 1-13.
25. Guillemaud T, Mieuzet L, Simon JC, (2003) Spatial and temporal genetic variability in French populations of the peach-potato aphid, Myzus persicae. Heredity, 91, 143-152.
26. Gurr GM, Wratten SD, Luna JM, (2003) Multi-function agricultural biodiversity: pest management and other benefits. Basic and Applied Ecology, 4, 107-116.
27. Hastie TJ, Pregibon D, (1992) Generalized linear models. In: Statistical Models in S (eds, Chambers JM, Hastie TJ,), pp. 195-247. Wadsworth & Brooks/Cole, Pacific Grove, California.
28. Hirao T, Murakami M, (2008) Quantitative food webs of lepidopteran leafminers and their parasitoids in a Japanese deciduous forest. Ecological Research, 23, 159-168.
29. Holt RD, (1977) Predation, apparent competition, and the structure of prey communities. Theoretical Population Biology, 12, 197-229.
30. Holt RD, Lawton JH, (1993) Apparent competition and enemy-free space in insect host-parasitoid communities. American Naturalist, 142, 623-645.
31. Holt RD, Lawton JH, (1994) The ecological consequences of shared natural enemies. Annual Review of Ecology and Systematics, 25, 495-520.
32. Iain SW, Dixon AFG, (2007) Life cycles and polymorphism. In: Aphids as Crop Pests (eds, van Emden HF, Harrington R,), pp. 69-86. CABI, Wallingford, Cambridge, UK.
33. Kaartinen R, Stone G, Hearn J, Lohse K, Roslin T, (2010) Revealing secret liaisons: DNA barcoding changes our understanding of food webs. Ecological Entomology, 35, 623-638.
34. Kavallieratos NG, Tomanovic Z, Starý P, et al,. (2004) A survey of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of Southeastern Europe and their aphid-plant associations. Applied Entomology and Zoology, 39, 527-563.
35. Klapwijk MJ, Lewis OT, (2011) Spatial ecology of multiple parasitoids of a patchily-distributed host: implications for species coexistence. Ecological Entomology, 36, 212-220.
36. Langer A, Hance T, (2004) Enhancing parasitism of wheat aphids through apparent competition: a tool for biological control. Agriculture, Ecosystems & Environment, 102, 205-212.
37. Lawton JH, (1986) The effect of parasitoids on phytophagous insect communities. In: Proceedings of the 13th Symposium of the Royal Entomological Society of London on Insect Parasitoids (eds, Waage J, Greathead D,), pp. 265-287. Academic Press, London, UK.
38. Lei GC, Hanski I, (1998) Spatial dynamics of two competing specialist parasitoids in a host metapopulation. Journal of Animal Ecology, 67, 422-433.
39. Lewis OT, Memmott J, Lasalle J, Lyal CHC, Whitefoord C, Godfray HCJ, (2002) Structure of a diverse tropical forest insect-parasitoid community. Journal of Animal Ecology, 71, 855-873.
40. Macfadyen S, Gibson R, Polaszek A, et al,. (2009) Do differences in food web structure between organic and conventional farms affect the ecosystem service of pest control? Ecology Letters, 12, 229-238.
41. May R, (2009) Food web assembly and collapse: mathematical models and implications for conservation. Philosophical Transactions of the Royal Society Biological Sciences, 364, 1643-1646.
42. Memmott J, Godfray HCJ, (1994) The use and construction of parasitoid webs. In: Parasitoid Community Ecology (ed., Sheehan W,), pp. 300-318. Oxford University Press, Oxford, UK.
43. Memmott J, Godfray HCJ, Gauld ID, (1994) The structure of a tropical host parasitoid community. Journal of Animal Ecology, 63, 521-540.
44. Morris RJ, Lewis OT, Godfray HCJ, (2004) Experimental evidence for apparent competition in a tropical forest food web. Nature, 428, 310-313.
45. Müller CB, Adriaanse ICT, Belshaw R, Godfray HCJ, (1999) The structure of an aphid-parasitoid community. Journal of Animal Ecology, 68, 346-370.
46. Peccoud J, Ollivier A, Plantegenest M, Simon JC, (2009) A continuum of genetic divergence from sympatric host races to species in the pea aphid complex. Proceedings of the National Academy of Sciences of the United States of America, 106, 7495-7500.
47. Petermann JS, Müller CB, Weigelt A, Weisser WW, Schmid B, (2010) Effect of plant species loss on aphid-parasitoid communities. Journal of Animal Ecology, 79, 709-720.
48. Pocock MJO, Evans DM, Memmott J, (2012) The robustness and restoration of a network of ecological networks. Science, 335, 973-977.
49. R Development Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
50. Rand TA, van Veen FJF, Tscharntke T, (2012) Landscape complexity differentially benefits generalized fourth, over specialized third, trophic level natural enemies. Ecography, 35, 97-104.
51. Rodriguez MA, Hawkins BA, (2000) Diversity, function and stability in parasitoid communities. Ecology letters, 3, 35-40.
52. Rosenheim JA, (1999) Higher-order predators and the regulation of insect herbivore populations. Annual Review of Entomology, 43, 421-447.
53. Rosenheim JA, Kaya HK, Ehler LE, Marois JJ, Jaffee BA, (1995) Intraguild predation among biological control agents: theory and evidence. Biological Control, 5, 303-335.
54. Rott AS, Godfray HCJ, (2000) The structure of a leafminer-parasitoid community. Journal of Animal Ecology, 69, 274-289.
55. Schönrogge K, Crawley M, (2000) Quantitative webs as a means of assessing the impact of alien insects. Journal of Animal Ecology, 69, 841-868.
56. Sha ZL, Zhu CD, Murphy RW, Huang DW, (2007) 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, 45, 128-135.
57. Shokralla S, Spall JL, Gibson JF, Hajibabaei M, (2012) Next-generation sequencing technologies for environmental DNA research. Molecular Ecology, 21, 1974-1805.
58. Starý P, (2006) Aphid Parasitoids of the Czech Republic. Akademie Ved Ceske Republiky, Czech Republic.
59. Storeck A, Poppy GM, van Emden HF, Powell W, (2000) The role of plant chemical cues in determining host preference in the generalist aphid parasitoid Aphidius colemani. Entomologia Experimentalis et Applicata, 97, 41-46.
60. Tack AJM, Gripenberg S, Roslin T, (2011) Can we predict indirect interactions from quantitative food webs?-an experimental approach. Journal of Animal Ecology, 80, 108-118.
61. Thébault E, Fontaine C, (2010) Stability of ecological communities and the architecture of mutualistic and trophic networks. Science, 329, 853-856.
62. Tomanovic Z, Kavallieratos NG, Starý P, et al,. (2003) Aphidius Nees aphid parasitoids (Hymenoptera, Braconidae, Aphidiinae) in Serbia and Montenegro: tritrophic associations and key. Acta Entomologica Serbica, 8, 15-39.
63. Tomic M, Tomanovic Z, Kavallieratos NG, et al,. (2005) Morphological variability of several biotypes of Ephedrus plagiator (Nees, 1811) (Hymenoptera: Braconidae: Aphidiinae) and description of a new species. Zoologischer Anzeiger, 244, 153-162.
64. Traugott M, Bell JR, Broad GR, Powell W, van Veen FF, (2008) Endoparasitism in cereal aphids: molecular analysis of a whole parasitoid community. Molecular Ecology, 17, 3928-3938.
65. Traugott M, Kamenova S, Ruess L, Plantegenest M, (2013) Empirically characterising trophic networks: what emerging DNA-based methods, stable isotope and fatty acid analyses can offer. Advances in Ecological Research, 49, 177-224.
66. Tscharntke T, Bommarco R, Clough Y, et al,. (2007) Conservation biological control and enemy diversity on a landscape scale. Biological Control, 43, 294-309.
67. Tylianakis JM, Tscharntke T, Lewis OT, (2007) Habitat modification alters the structure of tropical host-parasitoid food webs. Nature, 445, 202-205.
68. Valentini A, Pompanon F, Taberlet P, (2009) Barcoding for ecologists. Trends in ecology and evolution, 24, 110-117.
69. Valladares GR, Salvo A, Godfray HCJ, (2001) Quantitative food webs of dipteran leafminers and their parasitoids in Argentina. Ecological Research, 16, 925-939.
70. Vanlerberghe-Masutti F, Chavigny P, (1998) Host-based genetic differentiation in the aphid Aphis gossypii Glover, evidenced from RAPD fingerprints. Molecular Ecology, 7, 905-914.
71. van Veen FJF, Müller CB, Pell JK, Godfray HCJ, (2008) Food web structure of three guilds of natural enemies: predators, parasitoids and pathogens of aphids. Journal of Animal Ecology, 77, 191-200.
72. Vialatte A, Dedryver CA, Simon JC, Galman M, Plantegenest M, (2005) Limited genetic exchanges between populations of an insect pest living on uncultivated and related cultivated host plants. Proceedings of the Royal Society London Series B: Biological Sciences, 272, 1075-1082.
73. Walton MP, Powell W, Loxdale HD, Williams LA, (1990) Electrophoresis as a tool for estimating levels of hymenopterous parasitism in field populations of the cereal aphid, Sitobion avenae. Entomologia Experimentalis et Applicata, 54, 271-279.
74. von Zeipel H, Eriksson O, Ehrlen J, (2006) Host plant population size determines cascading effects in a plant-herbivore-parasitoid system. Basic and Applied Ecology, 7, 191-200.