Aphid galls accumulate high concentrations of amino acids: A support for the nutrition hypothesis for gall formation

Entomologia Experimentalis et Applicata

Volumn 113, Issue 1, 2004, Pages 35-44

  Koyama, Yoshitaka ^a   Yao, Izumi ^a   Akimoto, Shin Ichi ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Aphididae; EDTA; Glutamine; Homoptera; Nutrition; Phloem sap; Rhopalosiphum insertum; Sorbaphis chaetosiphon; Sorbus commixta

Indexed keywords

AMINO ACID; GALL INSECT; HYPOTHESIS TESTING; NUTRITION;

APHIDIDAE; HEMIPTERA; HEXAPODA; INSECTA; RHOPALOSIPHUM; RHOPALOSIPHUM INSERTUM; SORBUS; SORBUS COMMIXTA; VESPIDAE;

EID: 7244231276     PISSN: 00138703     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0013-8703.2004.00207.x     Document Type: Article

References (47)

1. Andersen PC & Mizell RF (1987) Physiological effects of galls induced by Phylloxera notabilis (Homoptera: Phylloxeridae) on pecan foliage. Environmental Entomology 16: 264-268.
2. Blackman RL & Eastop VF (1994) Aphids on the World's Trees. CAB International, Oxon, UK.
3. Brewer JW, Bishop JW & Skuhravy V (1987) Levels of foliar chemicals in insect-induced galls (Diptera: Cecidomyiidae). Journal of Applied Entomology 104: 504-510.
4. Dixon AFG (1998) Aphid Ecology, 2nd edn. Chapman & Hall, London.
5. Dorschner KW, Ryan JD, Johnson RC & Eikenbary RD (1987) Modification of host nitrogen levels by the greenbug (Homoptera: Aphididae): its role in resistance of winter wheat to aphids. Environmental Entomology 16: 1007-1011.
6. Douglas AE (1993) The nutritional quality of phloem sap utilized by natural aphid populations. Ecological Entomology 18: 31-38.
7. Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annual Review of Entomology 43: 17-37.
8. Flatt T & Weisser WW (2000) The effects of mutualistic ants on aphid life history traits. Ecology 81: 3522-3529.
9. Forrest JMS (1971) The growth of Aphis fabae as an indicator of the nutritional advantage of galling to the apple aphid Dysaphis devecta. Entomologia Experimentalis et Applicata 14: 477-483.
10. Girousse C & Bournoville R (1994) Role of phloem sap quality and exudation characteristics on performance of pea aphid grown on lucerne genotypes. Entomologia Experimentalis et Applicata 70: 227-235.
11. Hartley SE (1998) The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall-former? Oecologia 113: 492-501.
12. Hartley SE & Lawton JH (1992) Host-plant manipulation by gall-insects: a test of the nutrition hypothesis. Journal of Animal Ecology 61: 113-119.
13. Hodgson DJ & Godfray HCJ (1999) The consequences of clustering by Aphis fabae foundresses on spring migrant production. Oecologia 118: 446-452.
14. Hörtensteiner S & Feller U (2002) Nitrogen metabolism and remobilization during senescence. Journal of Experimental Botany 53: 927-937.
15. Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecological Monographs 54: 187-211.
16. Inbar M, Eshel A & Wool D (1995) Interspecific competition among phloem-feeding insects mediated by induced host-plant sinks. Ecology 76: 1506-1515.
17. Kamachi K, Yamaya T, Mae T & Ojima K (1991) A role for glutamine synthetase in the remobilization of leaf nitrogen during natural senescence in rice leaves. Plant Physiology 96: 411-417.
18. Karley AJ, Douglas AE & Parker WE (2002) Amino acid composition and nutritional quality of potato leaf phloem sap for aphids. Journal of Experimental Biology 205: 30090-33018.
19. King RW & Zeevaart JAD (1974) Enhancement of phloem exudation from cut petioles by chelating agents. Plant Physiology 53:96-103.
20. Kundu R & Dixon AFG (1995) Evolution of complex life cycles in aphids. Journal of Animal Ecology 64: 245-255.
21. Larson KC & Whitham TG (1991) Manipulation of food resources by a gall-forming aphid: the physiology of sink-source interactions. Oecologia 88: 15-21.
22. Larson KC & Whitham TG (1997) Competition between gall aphids and natural plant sinks: plant architecture affects resistance to galling. Oecologia 109: 575-582.
23. Leckstein PM & Llewellyn M (1974) The role of amino acids in diet intake and selection and the utilization of dipeptides by Aphis fabae. Journal of Insect Physiology 20: 877-885.
24. Maltais JB & Auclair JL (1962) Free amino acid and amide composition of pea leaf juice, pea aphid haemolymph, and honey-dew, following the rearing of aphids on single pea leaves treated with amino compounds. Journal of Insect Physiology 8: 391-399.
25. Mittler TE (1967) Effect on aphid feeding of dietary methionine. Nature 214: 386.
26. Nozawa A, Ito M, Hayashi H & Watanabe A (1999) Dark-induced expression of genes for asparagine synthetase and cytosolic glutamine synthetase in radish cotyledons is dependent on the growth stage. Plant Cell and Physiology 40: 942-948.
27. Petersen MK & Sandström JP (2001) Outcome of indirect competition between two aphid species mediated by responses in their common host plant. Functional Ecology 15: 525-534.
28. Price PW, Fernandes GW & Waring GL (1987) Adaptive nature of insect galls. Environmental Entomology 16: 15-24.
29. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43: 223-225.
30. Riedell WE (1989) Effect of Russian wheat aphid infestation on barley plant response to drought stress. Physiologia Plantarium 77: 587-592.
31. Sandström J (2000) Nutritional quality of phloem sap in relation to host plant-alternation in the bird cherry-oat aphid. Chemoecology 10: 17-24.
32. Sandström J & Pettersson J (1994) Amino acid composition of phloem sap and the relation to intraspecific variation in pea aphid (Acyrthosiphon pisum) performance. Journal of Insect Physiology 40: 947-955.
33. Sandström J, Telang A & Moran NA (2000) Nutritional enhancement of host plants by aphids - a comparison of three aphid species on grasses. Journal of Insect Physiology 46:33-40.
34. Sasaki T & Ishikawa H (1993) Nitrogen recycling in the endosymbiotic system of the pea aphid, Acyrthosiphon pisum. Zoological Science 10: 779-785.
35. Sasaki T & Ishikawa H (1995) Production of essential amino acids from glutamate by mycetocyte symbionts of the pea aphid, Acyrthosiphon pisum. Journal of Insect Physiology 41: 41-46.
36. Scheiner SM (2001) Theories, hypotheses, and statistics. Design and Analysis of Ecological Experiments (ed. by SM Scheiner & J Gurevitch), pp. 3-13, Oxford University Press, Oxford, UK.
37. Sokal RR & Rohlf FJ (1995) Biometry, 3rd edn. Freeman, New York.
38. Srivastava PN & Auclair JL (1975) Role of single amino acids in phagostimulation, growth and survivial of Acyrthosiphon pisum. Journal of Insect Physiology 21: 1865-1871.
39. Stadler B & Dixon AFG (1999) Ant attendance in aphids: why different degrees of myrmecophily? Ecological Entomology 24: 363-369.
40. Telang A, Sandström J, Dyreson E & Moran NA (1999) Feeding damage by Diuraphis noxia results in a nutritionally enhanced phloem diet. Entomologia Experimentalis et Applicata 91: 403-412.
41. Torikura H (1991) Revisional notes on Japanese Rhopalosiphum, with keys to species based on the morphs on the primary host. Japanese Journal of Entomology 59: 257-273.
42. Watanabe A, Takagi N, Hayashi H, Chino M & Watanabe A (1997) Internal Gln/Glu ratio as a potential regulatory parameter for the expression of a cytosolic glutamine synthetase gene of radish in cultured cells. Plant Cell and Physiology 38: 1000-1006.
43. Way MJ & Banks CJ (1967) Intra-specific mechanisms in relation to the natural regulation of numbers of Aphis fabae Scop. Annals of Applied Biology 59:189-205.
44. Weibull J, Ronquist F & Brishammar S (1990) Free amino acid composition of leaf exudates and phloem sap. Plant Physiology 92:222-226.
45. Weiner H, Blechschmidt-Schneider S, Mohme H, Eschrich W & Heldt HW (1991) Phloem transport of amino acids. Comparison of amino acid contents of maize leaves and of the sieve tube exudate. Plant Physiology and Biochemistry 29: 19-23.
46. Wilkinson TL & Douglas AE (2003) Phloem amino acids and the host plant range of the polyphagous aphid, Aphis fabae. Entomologia Experimentalis et Applicata 106: 103-113.
47. Wilson KA, McManus MT, Gordon ME & Jordan TW (2002) The proteomics of senescence in leaves of white clover, Trifolium repens (L.). Proteomics 2: 1114-1122.