Oecologia

, Volume 88, Issue 1, pp 15–21 | Cite as

Manipulation of food resources by a gall-forming aphid: the physiology of sink-source interactions

  • Katherine C. Larson
  • Thomas G. Whitham
Original Papers

Summary

We examined the capacity of the galling aphid, Pemphigus betae, to manipulate the sink-source translocation patterns of its host, narrowleaf cottonwood (Populus angustifolia). A series of 14C-labeling experiments and a biomass allocation experiment showed that P. betae galls functioned as physiologic sinks, drawing in resources from surrounding plant sources. Early gall development was dependent on aphid sinks increasing allocation from storage reserves of the stem, and later development of the progeny within the gall was dependent on resources from the galled leaf blade and from neighboring leaves. Regardless of gall position within a leaf, aphids intercepted 14C exported from the galled leaf (a non-mobilized source). However, only aphid galls at the most basal site of the leaf were strong sinks for 14C fixed in neighboring leaves (a mobilized source). Drawing resources from neighboring leaves represents active herbivore manipulation of normal host transport patterns. Neighboring leaves supplied 29% of the 14C accumulating in aphids in basal galls, while only supplying 7% to aphids in distal galls. This additional resource available to aphids in basal galls can account for the 65% increase in progeny produced in basal galls compared to galls located more distally on the leaf and limited to the galled leaf as a food resource. Developing furits also act as skins and compete with aphid-induced sinks for food supply. Aphid success in producing galls was increased 31% when surrounding female catkins were removed.

Key words

Galls Herbivory Sink-source Translocation Phloem-parasites 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Berenbaum M (1981) Patterns of furanocoumarin distribution and insect herbivory in the Umbelliferae: Plant chemistry and community structure. Ecology 62:1254–1266Google Scholar
  2. Billett EE, Burnett JH (1978) The host parasite physiology of the maize smut fungus Ustilago maydis. Part II: Translocation of C-14 labeled assimilates in smutted maize plants. Phys Plant Pathol 12:103–112Google Scholar
  3. Blescschmidt-Schneider S (1984) Conversion of mature leaves into sinks on the dicotyledonous C4 plants Amaranthus caudatus and Gomphrena globosa. Can J Bot 62:1081–1089Google Scholar
  4. Conn EE (1984) Compartmentation of secondary compounds. Ann Proc Phytochemical Soc Europe 24:1–28Google Scholar
  5. Cook MG, Evans LT (1983) The role of sink size and location in the partitioning of assimilates in wheat ears. Aust J Plant Physiol 10:313–327Google Scholar
  6. Craig TP, Price PW, Itami JK (1986) Resource regulation by a stem-galling sawfly on the arroyo willow. Ecology 67:419–425Google Scholar
  7. Dickson RE, Larson PR (1975) Incorporation of 14C-photosynthates into major chemical fractions of source and sink leaves of cottonwood. Plant Physiol 56:185–193Google Scholar
  8. Dickson RE, Larson PR (1981) 14C Fixation, metabolic labeling patterns, and translocation profiles during leaf development in Populus deltoides. Planta 152:461–470Google Scholar
  9. Dickson RE, Nelson EA (1982) Fixation and distribution of 14C in Populus deltoides during dormancy induction. Physiol Plant 54:393–401Google Scholar
  10. Dickson RE, Vogelmann TC, Larson PR (1985) Glutamine transfer from xylem to phloem and translocation to developing leaves of Populus deltoides. Plant Phys 77:412–417Google Scholar
  11. Egli DB, Guffy RD, Meckel LW, Leggett JE (1985) The effect of source-sink alterations on soybean seed growth. Ann Bot 55:395–402Google Scholar
  12. Feeny P (1976) Plant apparency and chemical defense. Rec Adv Phytochem 10:1–40Google Scholar
  13. Harris P (1980) Effects of Urophora affinis Frfld. and U. quadrifasciata (Meig.) (Diptera: Tephritidae) on Centaurea diffusa Lam. and C. maculosa Lam. (Compositae). Z Ang Ent 90:190–201Google Scholar
  14. Hartnett DC, Bazzaz FA (1984) Leaf demography and plant-insect interactions: goldenrods and phloem-feedings aphids. Am Nat 124:137–142Google Scholar
  15. Ho LC (1988) Metabolism and compartmentation of imported sugars in sink organs in relation to sink strength. Ann Rev. Plant Physiol Plant Mol Biol 39:355–378Google Scholar
  16. Isebrands JG, Larson PR (1973) Anatomical changes during leaf ontogeny in Populus deltoides. Am J Bot 60:199–208Google Scholar
  17. Isebrands JG, Larson PR (1977) Organization and ontogeny of the vascular system in the petiole of eastern cottonwood. Amer J Bot 64:65–77Google Scholar
  18. Isebrands JG, Nelson ND (1983) Distribution of 14C-labeled photosynthates within intensively cultured Populus clones during the establishment year. Physiol Plant 59:9–18Google Scholar
  19. Kearsley MJC, Whitham TG (1989) Developmental changes in resistance to herbivory: implications for individuals and populations. Ecology 70:422–434Google Scholar
  20. Larew HG (1981) A comparative anatomical study of galls caused by the major cecidogenic groups, with special emphasis on the nutritive tissue. PhD thesis, Oregon State Univ., CorvallisGoogle Scholar
  21. Larson PR, Dickson RE (1973) Distribution of imported 14C in developing leaves of eastern cottonwood according to phyllotaxy. Planta 111:95–112Google Scholar
  22. Larson PR, Isebrands JG, Dickson RE (1980) Sink to source transition of Populus leaves. Ber Deutsch Bot Ges 93:79–80Google Scholar
  23. Larsson S (1985) Seasonal changes in the within-crown distribution of the aphid Cinara pini on Scots pine. Oikos 35:217–222Google Scholar
  24. McCrea KD, Abrahamson WG, Weis AE (1985) Goldenrod ball gall effects of Solidago altissima: 14C translocation and growth. Ecology 66:1902–1907Google Scholar
  25. McKey D (1979) The distribution of secondary compounds within plants. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interactions with secondary plant metabolites. Academic Press, New York, pp 56–133Google Scholar
  26. Mullin GA (1986) Adaptive divergence of chewing and sucking arthropods to plant allelochemicals. In: Brattsten L, Ahmad S (eds) Molecular aspects of insect-plant associations. Plenum Press, New York, pp 175–209Google Scholar
  27. Price PW, Roininen H, Tahvanainen J (1987) Why does the budgalling sawfly, Euura mucronata, attack long shoots?Google Scholar
  28. Raven P (1983) Phytophages of xylem and phloem. Rec Adv Ecol 14:136–234Google Scholar
  29. Rhoades DF, Cates RG (1976) Toward a general theory of plant antiherbivore chemistry. Rec Adv Phytochem 10:168–213Google Scholar
  30. Rohfritsch O (1987) Different food supply strategies in midge induced plant galls. In: Labeyrie V, Fabres G, Lachaise D (eds) Insects-plants. W Junk Publishers, Dordrecht, pp 195–200Google Scholar
  31. Rosenthal GA, Janzen DH (1979) Herbivores: their interactions with secondary plant metabolites. Academic Press, New YorkGoogle Scholar
  32. Sharma V, Strack D (1985) Vacuolar localization of 1-sinapolyglucose: L-malate sinapolytransferase in protoplasts from cotyledons of Raphanus sativus. Planta 163:563–568Google Scholar
  33. Shorthouse JD, West A, Landry RW, Thibodeau PD (1986) Structural damage by female Hemadas nubilipennis (Hymenoptera: Pteromalidae) as a factor in gall induction on lowbush blueberry. Can Ent 118:249–254Google Scholar
  34. Sutton RD (1984) The effect of host plant flowering on the distribution and growth of hawthorn psyllids (Homoptera: Psylloidea). J Anim Ecol 53:37–50Google Scholar
  35. Taper ML, Case TJ (1987) Interactions between oak tannins and parasite community structure: unexpected benefits of tannins to cynipid gall-wasps. Oecologia 71:254–261Google Scholar
  36. Thrower SL (1974) Sink limitation and import of assimilate into mature leaves. New Phyt 73:685–687Google Scholar
  37. Vogelmann TC, Larson PR, Dickson RE (1982) Translocation pathways in the petioles and stem between source and sink leaves of Populus deltoides Bartr. ex Marsh. Planta 156:345–358Google Scholar
  38. Wareing PF, Patrick J (1975) Source-sink relations and the partition of assimilates in the plant. In: Cooper J (ed) Photosynthesis and productivity in different environments. Cambridge Univ Press, Cambridge, pp 481–499Google Scholar
  39. Waring GL, Price PW, (1988) Consequences of host plant chemical and physical variability to an associated herbivore. Ecol Res 3:205–216Google Scholar
  40. Watson MA, Casper B (1984) Morphogenetic constraints on patterns of carbon distribution in plants. Ann Rev Ecol Syst 15:233–258Google Scholar
  41. Way MJ, Cammell M (1970) Aggregation behaviour in relation of food utilization by aphids. In: Watson A (ed) Animal populations in relation to their food resources, Blackwell, Oxford, pp 229–246Google Scholar
  42. Weis AE (1984) Apical dominance asserted over lateral buds by the gall of Rhabdophaga strobiloides (Diptera: Cecidomyiidae). Can Ent 116:1277–1279Google Scholar
  43. Weis AE, Kapelinski A (1984) Manipulation of host plant development by the gall-midge Rhabdophaga strobiloides. Ecol Ent 9:457–465Google Scholar
  44. Whitham TG (1978) Habitat selection by Pemphigus aphids in response to resource limitation and competition. Ecology 59:1164–1176Google Scholar
  45. Whitham TG (1986) Costs and benefits of territoriality: behavioral and reproductive release by competing aphids. Ecology 67:139–147Google Scholar
  46. Williams AG, Whitham TG (1986) Premature leaf abscission; and induced plant defense against gall aphids. Ecology 67:1619–1627Google Scholar
  47. Wratten SD (1974) Aggregation in the birch aphid Euceraphis punctipennis (Zett.) in relation to food quality. Anim Ecol 43:191–198Google Scholar
  48. Wratten SD, Edwards DJ, Dunn I (1984) Wound induced changes in the palatability of Betula pubescens and B. pendula Oecologia 61:372–375Google Scholar
  49. Wu A, Thrower LB (1981) The physiological association between Aphis craccivora Koch and Vigna sesquipedalis Fruw. New Phyt 88:89–102Google Scholar
  50. Wyse RE (1986) Sinks as determinants of assimilate partitioning: possible sites for regulation. In: Cronshaw J, Lucas WJ, Giaquinta RT (eds) Phloem transport, Alan R. Liss, New York. pp 197–210Google Scholar
  51. Zucker WV (1982) How aphids choose leaves: the roles of phenolics in host selection by a galling aphid. Ecology 63:972–981Google Scholar

Copyright information

© Springer-Verlag 1991

Authors and Affiliations

  • Katherine C. Larson
    • 1
  • Thomas G. Whitham
    • 1
  1. 1.Department of Biological SciencesNorthern Arizona UniversityFlagstaffUSA

Personalised recommendations