Large interclone differences in melezitose secretion in the facultatively ant-tended black bean aphid Aphis fabae

Journal of Insect Physiology

Volumn 57, Issue 12, 2011, Pages 1614-1621

  Vantaux, A ^a   Van den Ende, W ^a   Billen, J ^a   Wenseleers, T ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Ant aphid mutualism; Ant attendance; Black bean aphid; Carbohydrate biosynthesis; Honeydew sugar composition

Indexed keywords

MELEZITOSE; TRISACCHARIDE;

ADAPTATION; ANT; APHID; CARBOHYDRATE; CLONE; EVOLUTIONARY BIOLOGY; HONEYDEW; MUTUALISM; NATURAL ENEMY; SECRETION; SUGAR;

ANIMAL; ANT; APHID; ARTICLE; CARBOHYDRATE METABOLISM; COMPARATIVE STUDY; PHYSIOLOGY; SECRETION; SYMBIOSIS;

ANIMALS; ANTS; APHIDS; CARBOHYDRATE METABOLISM; SYMBIOSIS; TRISACCHARIDES;

APHIDIDAE; APHIS FABAE; CUCUMIS MELO VAR. INODORUS; FORMICIDAE; HEXAPODA;

EID: 82555164912     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2011.08.014     Document Type: Article

References (74)

1. Ashford D.A., Smith W.A., Douglas A.E. Living on a high sugar diet: the fate of sucrose ingested by a phloem-feeding insect, the pea aphid Acyrthosiphon pisum. Journal of Insect Physiology 2000, 46:335-341.
2. Auclair J.L. Aphid feeding and nutrition. Annual Review of Entomology 1963, 8:439-490.
3. Banks C.J. Effects of the ant Lasius niger (L.) on insects preying on small populations of Aphis fabae Scop on bean plants. Annals of Applied Biology 1962, 50:669-679.
4. Becerra J.X.I., Venable D.L. Extrafloral nectaries: a defense against ant-Homoptera mutualisms?. Oikos 1989, 55:276-280.
5. Blüthgen N., Fiedler K. Preferences for sugars and amino acids and their conditionality in a diverse nectar-feeding ant community. Journal of Animal Ecology 2004, 73:155-166.
6. Blüthgen N., Gottsberger G., Fiedler K. Sugar and amino acid composition of ant-attended nectar and honeydew sources from an Australian rainforest. Austral Ecology 2004, 29:418-429.
7. Boevé J.L., Wäckers F.L. Gustatory perception and metabolic utilization of sugars by Myrmica rubra ant workers. Oecologia 2003, 136:508-514.
8. Boucher D.H. The Biology of Mutualism: Ecology and Evolution 1988, Oxford University Press.
9. Braendle C., Weisser W.W. Variation in escape behavior of red and green clones of the pea aphid. Journal of Insect Behavior 2001, 14:497-509.
10. Bristow C.M. Why are so few aphids ant-tended?. Ant-Plant Interactions 1991, Oxford University Press. C.R. Huxley, D.F. Cutler (Eds.).
11. Bronstein J.L. Our current understanding of mutualism. Quarterly Review of Biology 1994, 69:31-51.
12. Byrne D.N., Miller W.B. Carbohydrate and amino-acid composition of phloem sap and honeydew produced Bemisia tabaci. Journal of Insect Physiology 1990, 36:433-439.
13. Cornelius M.L., Grace J.K., Yates J.R. Acceptability of different sugars and oils to three tropical ant species (Hymen, Formicidae). Anzeiger Fur Schadlingskunde Pflanzenschutz Umweltschutz 1996, 69:41-43.
14. Cristofoletti P.T., Ribeiro A.F., Deraison C., Rahbe Y., Terra W.R. Midgut adaptation and digestive enzyme distribution in a phloem feeding insect, the pea aphid Acyrthosiphon pisum. Journal of Insect Physiology 2003, 49:11-24.
15. Cushman J.H., Addicott J.F. Intra- and interspecific competition for mutualists: ants as a limited and limiting resource for aphids. Oecologia 1989, 79:315-321.
16. Detrain C., Verheggen F.J., Diez L., Wathelet B., Haubruge E. Aphid-ant mutualism: how honeydew sugars influence the behaviour of ant scouts. Physiological Entomology 2010, 35:168-174.
17. Dinant S. Phloem, transport between organs and long-distance signalling. Comptes Rendus Biologies 2008, 331:334-346.
18. Dixon A.F.G., Agarwala B.K. Ladybird-induced life-history changes in aphids. Proceedings of the Royal Society of London Series B-Biological Sciences 1999, 266:1549-1553.
19. Douglas A.E. Provenance, experience and plant utilisation by the polyphagous aphid, Aphis fabae. Entomologia Experimentalis et Applicata 1997, 83:161-170.
20. Douglas, A.E., 2003. The nutritional physiology of aphids, Advances in Insect Physiology 31,73-140.
21. Douglas A.E. Phloem-sap feeding by animals: problems and solutions. Journal of Experimental Botany 2006, 57:747-754.
22. Duckett D.P. Further studies of ant-aphid interactions 1974, Imperial College, University of London, London.
23. Engel V., Fischer M.K., Wäckers F.L., Völkl W. Interactions between extrafloral nectaries, aphids and ants: are there competition effects between plant and homopteran sugar sources?. Oecologia 2001, 129:577-584.
24. Fiehn O. Metabolic networks of Cucurbita maxima phloem. Phytochemistry 2003, 62:875-886.
25. Fischer M.K., Hoffmann K.H., Völkl W. Competition for mutualists in an ant-Homopteran interaction mediated by hierarchies of ant attendance. Oikos 2001, 92:531-541.
26. Fischer M.K., Shingleton A.W. Host plant and ants influence the honeydew sugar composition of aphids. Functional Ecology 2001, 15:544-550.
27. Fischer M.K., Völkl W., Hoffmann K.H. Honeydew production and honeydew sugar composition of polyphagous black bean aphid, Aphis fabae (Hemiptera: Aphididae) on various host plants and implications for ant-attendance. European Journal of Entomology 2005, 102:155-160.
28. Fischer M.K., Völkl W., Schopf R., Hoffmann K.H. Age-specific patterns in honeydew production and honeydew composition in the aphid Metopeurum fuscoviride: implications for ant-attendance. Journal of Insect Physiology 2002, 48:319-326.
29. Fisher D.B., Wright J.P., Mittler T.E. Osmoregulation by the aphid Myzus persicae: a physiological role for honeydew oligosaccharides. Journal of Insect Physiology 1984, 30:387.
30. Gorur G., Lomonaco C., Mackenzie A. Phenotypic plasticity in host-plant specialisation in Aphis fabae. Ecological Entomology 2005, 30:657-664.
31. Hausmann C., Wäckers F.L., Dorn S. Sugar convertibility in the parasitoid Cotesia glomerata (Hymenoptera: Braconidae). Archives of Insect Biochemistry and Physiology 2005, 60:223-229.
32. Hendrix D.L., Wei Y.A., Leggett J.E. Homopteran honeydew sugar composition is determined by both the insect and plant species. Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology 1992, 101:23-27.
33. Henneberry T.J., Jech L.F., de la Torre T., Hendrix D.L. Cotton aphid (Homoptera: Aphididae) biology, honeydew production, sugar quality and quantity, and relationships to sticky cotton. Southwestern Entomologist 2000, 25:161-174.
34. Hogervorst P.A.M., Wackers F.L., Romeis J. Effects of honeydew sugar composition on the longevity of Aphidius ervi. Entomologia Experimentalis et Applicata 2007, 122:223-232.
35. Hogervorst P.A.M., Wäckers F.L., Romeis J. Detecting nutritional state and food source use in field-collected insects that synthesize honeydew oligosaccharides. Functional Ecology 2007, 21:936-946.
36. Hölldobler B., Wilson E.O. The Ants 1990, Springer-Verlag, Berlin.
37. Ide T., Suzuki N., Katayama N. The use of honeydew in foraging for aphids by larvae of the ladybird beetle, Coccinella septempunctata L. (Coleoptera: Coccinellidae). Ecological Entomology 2007, 32:455-460.
38. Karley A.J., Ashford D.A., Minto L.M., Pritchard J., Douglas A.E. The significance of gut sucrase activity for osmoregulation in the pea aphid, Acyrthosiphon pisum. Journal of Insect Physiology 2005, 51:1313-1319.
39. Katayama N., Suzuki N. Extrafloral nectaries indirectly protect small aphid colonies via ant-mediated interactions. Applied Entomology and Zoology 2010, 45:505-511.
40. Kennedy J.S., Stroyan H.L.G. Biology of aphids. Annual Review of Entomology 1959, 4:139-160.
41. Kiss A. Melezitose, aphids and ants. Oikos 1981, 37:382.
42. Kunert G., Otto S., Rose U.S.R., Gershenzon J., Weisser W.W. Alarm pheromone mediates production of winged dispersal morphs in aphids. Ecology Letters 2005, 8:596-603.
43. Majerus M.E.N., Sloggett J.J., Godeau J.F., Hemptinne J.L. Interactions between ants and aphidophagous and coccidophagous ladybirds. Population Ecology 2007, 49:15-27.
44. Matsuura K., Yashiro T. Aphid egg protection by ants: a novel aspect of the mutualism between the tree-feeding aphid Stomaphis hirukawai and its attendant ant Lasius productus. Naturwissenschaften 2006, 93:506-510.
45. Minarro M., Fernandez-Mata G., Medina P. Role of ants in structuring the aphid community on apple. Ecological Entomology 2010, 35:206-215.
46. Müller F.P. Differential alarm pheromone responses between strains of the aphid Acyrthosiphon pisum. Entomologia Experimentalis et Applicata 1983, 34:347-348.
47. Nielsen C., Agrawal A.A., Hajek A.E. Ants defend aphids against lethal disease. Biology Letters 2010, 6:205-208.
48. Price D.R.G., Karley A.J., Ashford D.A., Isaacs H.V., Pownall M.E., Wilkinson H.S., Gatehouse J.A., Douglas A.E. Molecular characterisation of a candidate gut sucrase in the pea aphid, Acyrthosiphon pisum. Insect Biochemistry and Molecular Biology 2007, 37:307-317.
49. Price D.R.G., Tibbles K., Shigenobu S., Smertenko A., Russell C.W., Douglas A.E., Fitches E., Gatehouse A.M.R., Gatehouse J.A. Sugar transporters of the major facilitator superfamily in aphids; from gene prediction to functional characterization. Insect Molecular Biology 2010, 19:97-112.
50. Rhodes J.D., Croghan P.C., Dixon A.F.G. Dietary sucrose and oligosaccharide synthesis in relation to osmoregulation in the pea aphid, Acyrthosiphon pisum. Physiological Entomology 1997, 22:373-379.
51. Sachs J.L., Mueller U.G., Wilcox T.P., Bull J.J. The evolution of cooperation. Quarterly Review of Biology 2004, 79:135-160.
52. Schwartzberg E.G., Kunert G., Roese U.S.R., Gershenzon J., Weisser W.W. Alarm pheromone emission by pea aphid, Acyrthosiphon pisum, clones under predation by lacewing larvae. Entomologia Experimentalis et Applicata 2008, 128:403-409.
53. Stadler B. The relative importance of host plants, natural enemies and ants in the evolution of life-history characters in aphids. Vertical Food Web Interactions 1997, 241-256. Springer Verlag, Berlin. K. Dettner, G. Bauer, W. Völkl (Eds.).
54. Stadler B., Dixon A.F.G. Costs of ant attendance for aphids. Journal of Animal Ecology 1998, 67:454-459.
55. Stadler B., Dixon A.F.G. Ecology and evolution of aphid-ant interactions. Annual Review of Ecology Evolution and Systematics 2005, 36:345-372.
56. Stroyan H.L.G. Aphids-Pterocommatinae and Aphidinae (Aphidini), Homoptera, Aphididae 1984, Royal Entomological Society of London, London.
57. Tosh C.R., Powell G., Hardie J. Decision making by generalist and specialist aphids with the same genotype. Journal of Insect Physiology 2003, 49:659-669.
58. Van den Ende W., Mintiens A., Speleers H., Onuoha A.A., Van Laere A. The metabolism of fructans in roots of Cichorium intybus during growth, storage and forcing. New Phytologist 1996, 132:555-563.
59. Vantaux, A., Billen, J., Wenseleers, T., 2011. Levels of clonal mixing in the black bean aphid Aphis fabae, a facultative ant mutualist. Molecular Ecology doi:. doi:10.1111/j.1365-294X.2011.05204.x.
60. Völkl W., Woodring J., Fischer M., Lorenz M.W., Hoffmann K.H. Ant-aphid mutualisms: the impact of honeydew production and honeydew sugar composition on ant preferences. Oecologia 1999, 118:483-491.
61. Wäckers F.L. Gustatory response by the hymenopteran parasitoid Cotesia glomerata to a range of nectar and honeydew sugars. Journal of Chemical Ecology 1999, 25:2863-2877.
62. Wäckers F.L. Do oligosaccharides reduce the suitability of honeydew for predators and parasitoids? A further facet to the function of insect-synthesized honeydew sugars. Oikos 2000, 90:197-201.
63. Wäckers F.L. A comparison of nectar- and honeydew sugars with respect to their utilization by the hymenopteran parasitoid Cotesia glomerata. Journal of Insect Physiology 2001, 47:1077-1084.
64. Wäckers F.L., van Rijn P.C.J., Heimpel G.E. Honeydew as a food source for natural enemies: making the best of a bad meal?. Biological Control 2008, 45:176-184.
65. Way M.J. Mutualism between ants and honeydew-producing Homoptera. Annual Review of Entomology 1963, 8:307-344.
66. Weil J.-H. Biochimie Générale 1978, Masson, Paris.
67. Wilkinson T.L., Ashford D.A., Pritchard J., Douglas A.E. Honeydew sugars and osmoregulation in the pea aphid Acyrthosiphon pisum. Journal of Experimental Biology 1997, 200:2137-2143.
68. Woodring J., Wiedemann R., Fischer M.K., Hoffmann K.H., Völkl W. Honeydew amino acids in relation to sugars and their role in the establishment of ant-attendance hierarchy in eight species of aphids feeding on tansy (Tanacetum vulgare). Physiological Entomology 2004, 29:311-319.
69. Woodring J., Wiedemann R., Völkl W., Hoffmann K.H. Oligosaccharide synthesis regulates gut osmolality in the ant-attended aphid Metopeurum fuscoviride but not in the unattended aphid Macrosiphoniella tanacetaria. Journal of Applied Entomology 2007, 131:1-7.
70. Wool D., Hendrix D.L., Shukry O. Seasonal variation in honeydew sugar content of galling aphids (Aphidoidea: Pemphigidae: Fordinae) feeding on Pistacia: host ecology and aphid physiology. Basic and Applied Ecology 2006, 7:141-151.
71. Wyckhuys K.A.G., Strange-George J.E., Kulhanek C.A., Wäckers F.L., Heimpel G.E. Sugar feeding by the aphid parasitoid Binodoxys communis: How does honeydew compare with other sugar sources?. Journal of Insect Physiology 2008, 54:481-491.
72. Yao I., Akimoto S. Ant attendance changes the sugar composition of the honeydew of the drepanosiphid aphid Tuberculatus quercicola. Oecologia 2001, 128:36-43.
73. Yao I., Akimoto S.I. Flexibility in the composition and concentration of amino acids in honeydew of the drepanosiphid aphid Tuberculatus quercicola. Ecological Entomology 2002, 27:745-752.
74. Yao I., Shibao H., Akimato S. Costs and benefits of ant attendance to the drepanosiphid aphid Tuberculatus quercicola. Oikos 2000, 89:3-10.