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Evolutionary Ecology

, Volume 11, Issue 4, pp 419–437 | Cite as

Why are there no small species among xylem-sucking insects?

  • Vojtech Novotny
  • Michael R. Wilson
Article

Abstract

Xylem-sucking herbivores must cope with negative tension and extremely low nutrient concentration of xylem fluid. We test the hypothesis that the energetic cost of xylem fluid extraction grows with decreasing body size, as small species have relatively high metabolic rates and small feeding apparatus. The suction pressure gradient needed for feeding (P), calculated using Poiseuille's Law, and the cibarial pump load (L), estimated as xylem fluid volume per unit volume of cibarial muscles, were used to quantify energetic costs associated with feeding. Interspecific relationships between body size and frontoclypeus (cibarial pump) volume, proboscis length and food canal diameter were quantified using the structural relations model and model I (‘ordinary’) regressions applied on species as data points (phylogeny ignored), and on independent (intrageneric) contrasts (taxonomy used as a surrogate of phylogeny). All the dimensions of feeding apparatus changed approximately isometrically with body volume. In consequence, the suction pressure gradient P∼ (body volume)−0.21, and the cibarial pump load L∼ (body volume)−0.17. These relationships result in an allometric change in energetic costs associated with xylem feeding. Energy needed to overcome the resistance of feeding apparatus (P) becomes negligible for any species longer than about 8mm, and there is an important decrease in the L values in species over about 17mm in body length. These allometric trends can result in large species having a wider range of potential (energetically profitable) host plants than small species. Analysis of body size distributions in xylem-feeding insects, which all belong to the Auchenorrhyncha (Hemiptera), showed that xylem feeders tend to be larger than phloem feeders, especially in terms of the minimum body size. Two evolutionary transitions from phloem to xylem feeding in Hemiptera were associated with an increase in the minimum body size. A possibility that the evolution of minimum body size in xylem feeders is energetically constrained is discussed.

allometry body size constraint Hemiptera herbivores host plant insects phylogeny Poiseuille's Law regression xylem sap 

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References

  1. Andersen, P.C., Brodbeck, B.V. and Mizell, R.F. III. (1989) Metabolism of amino acids, organic acids and sugars extracted from the xylem fluid of four host plants by adult Homalodisca coagulata. Entomol. Exp. Appl. 50, 149–159.CrossRefGoogle Scholar
  2. Andersen, P.C., Brodbeck, B.V. and Mizell, R.F. III. (1992) Feeding by the leafhopper, Homalodisca coagulata, in relation to xylem fluid chemistry and tension. J. Insect Physiol. 38, 611–622.CrossRefGoogle Scholar
  3. Andrzejewska, L. (1967) Estimation of the effects of feeding of the sucking insect Cicadella viridis L. (Homoptera — Auchenorrhyncha) on plants. In Secondary Productivity of Terrestrial Ecosystems (K. Petrusewicz, ed.), pp. 791–805. Polish Academy of Science, Warsaw.Google Scholar
  4. Backus, E.A. (1985) Anatomical and sensory mechanisms of leafhopper and planthopper feeding behavior. In The Leafhoppers and Planthoppers (L.R. Nault and J.G. Rodriguez, eds), pp. 163–194. Wiley Interscience, New York.Google Scholar
  5. Backus, E.A. (1988) Sensory systems and behaviours which mediate hemipteran plant-feeding: A taxonomic overview. J. Insect Physiol. 3, 151–165.CrossRefGoogle Scholar
  6. Brodbeck, V.B., Mizell, R.F. III, French, W.J., Andersen, P.C. and Aldrich, J.H. (1990) Amino acids as determinants of host preference for the xylem feeding leafhopper, Homalodisca coagulata (Homoptera: Cicadellidae). Oecologia 83, 338–345.Google Scholar
  7. Brodbeck, V.B., Mizell, R.F. III and Andersen, P.C. (1993) Physiological and behavioral adaptations of three species of leafhoppers in response to the dilute nutrient content of xylem fluid. J. Insect Physiol. 39, 73–81.CrossRefGoogle Scholar
  8. Brown, J.H. and Maurer, B.A. (1989) Macroecology: The division of food and space among species on continents. Science 243, 1145–1150.Google Scholar
  9. Brown, J.H. and Nicoletto, P.F. (1991) Spatial scaling of species composition: Body masses of North American land mammals. Am. Nat. 138, 1478–1512.CrossRefGoogle Scholar
  10. Calder, W.A. III (1984) Size, Function, and Life History. Harvard University Press, Cambridge, MA.Google Scholar
  11. Carver, M., Gross, G.F. and Woodward, T.E. (1991) Hemiptera. In The Insects of Australia, 2nd edn, pp. 429–509. Melbourne University Press, Carlton.Google Scholar
  12. Cheung, W.W.K. and Marshall, A.T. (1973) Water and ionic regulation in cicadas in relation to xylem feeding. J. Insect Physiol. 19, 1801–1816.CrossRefGoogle Scholar
  13. Claridge, M.F. and Wilson, M.R. (1981) Host plant associations, diversity and species-area relationships of mesophyll-feeding leafhoppers of trees and shrubs in Britain. Ecol. Entomol. 6, 217–238.Google Scholar
  14. Cobben, R.H. (1988) What do we really know about host selection in Auchenorrhyncha? In Proceedings of the 6th Auchenorrhyncha Meeting (C. Vidano and A. Arzone, eds), pp. 81–92. IPRA, Turin.Google Scholar
  15. Demment, M.W. and Van Soest, P.J. (1985) A nutritional explanation for body-size patterns of ruminant and nonruminant herbivores. Am. Nat. 125, 641–672.CrossRefGoogle Scholar
  16. Distant, W.L. (1906) The Fauna of British India Including Ceylon and Burma: Rhynchota — Vol. 3. Heteroptera — Homoptera. Taylor and Francis, London.Google Scholar
  17. Distant, W.L. (1908) The Fauna of British India Including Ceylon and Burma: Rhynchota — Vol. 4. Homoptera: Appendix. Taylor and Francis, London.Google Scholar
  18. Distant, W.L. (1916) The Fauna of British India Including Ceylon and Burma: Rhynchota — Vol. 6. Homoptera: Appendix. Taylor and Francis, London.Google Scholar
  19. Distant, W.L. (1918) The Fauna of British India Including Ceylon and Burma: Rhynchota — Vol. 7. Homoptera: Appendix and Heteroptera: Addenda. Taylor and Francis, London.Google Scholar
  20. Dixon, A.F.G., Kindlmann, P. and Jarosik, V. (1995) Body size distribution in aphids: Relative surface area of specific plant structures. Ecol. Entomol. 20, 111–117.Google Scholar
  21. Dixon, A.F.G. and Kindlmann, P. (submitted) Cost of flight apparatus and optimum body size in insect migrants. Ecology.Google Scholar
  22. Emelyanov, A.F. (1987) Phylogeny of the plant hoppers based on the comparative morphological data. Trudy Vsesoyuz. Entomol. Obshch. 69, 19–109 (in Russian).Google Scholar
  23. Evans, J.W. (1977) The leafhoppers and froghoppers of Australia and New Zealand (Homoptera: Cicadelloidea and Cercopidea). Part 2. Rec. Austral. Mus. 31, 83–129.Google Scholar
  24. Field, C.B. and Holbrook, N.M. (1989) Catastrophic xylem failure: Tree life at the brink. TREE 4, 124–126.Google Scholar
  25. Forbes, A.R. and Raine, J. (1973) The stylets of the six-spotted leafhopper, Macrosteles fascifrons (Homoptera: Cicadellidae). Can. Ent. 105, 559–567.Google Scholar
  26. Gaston, K. J. (1991) Body size and probability of description: The beetle fauna of Britain. Ecol. Entomol. 16, 505–508.Google Scholar
  27. Gaston, K.J. and Reavey, D. (1989) Patterns in the life histories and feeding strategies of British macrolepidoptera. Biol. J. Linn. Soc. 37, 367–381.Google Scholar
  28. Gunthardt, M.S. and Wanner, H. (1981) The feeding behaviour of two leafhoppers on Vicia faba. Ecol. Entomol. 6, 17–22.Google Scholar
  29. Hamilton, K.G.A. (1981) Morphology and evolution of the rhynchotan head (Insecta: Hemiptera, Homoptera). Can. Entomol. 113, 953–974.Google Scholar
  30. Hamilton, K.G.A. (1982) The Spittlebugs of Canada. Homoptera: Cercopidae. Canadian Government Publishing Centre, Ottawa.Google Scholar
  31. Hamilton, K.G.A. (1983) Classification, morphology and phylogeny of the family Cicadellidae (Rhynchota: Homoptera). In 1st International Workshop on Leafhoppers and Planthoppers of Economic Importance (W.J. Knight, N.C. Pant, T.S. Robertson and M.R. Wilson, eds), pp. 15–37. CAB, London.Google Scholar
  32. Hanken, J. and Wake, D.B. (1993) Miniaturization of body size: Organismal consequences and evolutionary significance. Ann. Rev. Ecol. Syst. 24, 501–519.CrossRefGoogle Scholar
  33. Harvey, P.M. and Pagel, M.D. (1991) The Comparative Method in Evolutionary Biology. Oxford University Press, New York.Google Scholar
  34. Hodkinson, I.D. and Casson, D. (1991) A lesser predilection for bugs: Hemiptera (Insecta) diversity in tropical rain forests. Biol. J. Linn. Soc. 43, 101–109.Google Scholar
  35. Hoffman, G.D. and McEvoy, P.B. (1986) Mechanical limitations on feeding by meadow spittlebugs Philaenus spumarius (Homoptera: Cercopidae) on wild and cultivated host plants. Ecol. Entomol. 11, 415–426.Google Scholar
  36. Horsfield, D. (1977) Relationships between feeding of Philaenus spumarius (L.) and the amino acid concentration in the xylem sap. Ecol. Entomol. 2, 259–266.Google Scholar
  37. Horsfield, D. (1978) Evidence for xylem feeding by Philaenus spumarius (L.) (Homoptera: Cercopidae). Entomol. Exp. Appl. 24, 95–99.CrossRefGoogle Scholar
  38. Houston, B.R., Esau, K. and Hewitt, W.B. (1947) The mode of vector feeding and the tissues involved in the transmission of Pierce's disease virus in grape and alfalfa. Phytopathology 37, 247–253.Google Scholar
  39. Kabrick, L.R. and Backus, E.A. (1990) Salivary deposits and plant damage associated with specific probing behaviors of the potato leafhopper, Empoasca fabae, on alfalfa stems. Ent. Exp. Appl. 56, 287–304.CrossRefGoogle Scholar
  40. Karban, R. (1986) Prolonged development in cicadas. In Evolution of Insect Life Histories (F. Taylor and R. Karban, eds), pp. 222–235. Springer, New York.Google Scholar
  41. La Barbera, M. (1989) Analyzing body size as a factor in ecology and evolution. Ann. Rev. Ecol. Syst. 20, 97–117.CrossRefGoogle Scholar
  42. Lindstrom, J., Kaila, L. and Niemela, P. (1994) Polyphagy and adult body size in geometrid moths. Oecologia 98, 130–132.CrossRefGoogle Scholar
  43. Llewellyn, M. (1982) The energy economy of fluid-feeding herbivorous insects. In Proceedings of the 5th International Symposium on Insect-Plant Relationships, pp. 243–251. Pudoc, Wageningen.Google Scholar
  44. Mattson, W.J. (1980) Herbivory in relation to plant nitrogen content. Ann. Rev. Ecol. Syst. 11, 119–161.CrossRefGoogle Scholar
  45. McKitrick, M.C. (1993) Phylogenetic constraint in evolutionary theory: Has it any explanatory power? Ann. Rev. Ecol. Syst. 24, 307–330.CrossRefGoogle Scholar
  46. Mittler, T.E. (1967) Water tension in plants — an entomological approach. Ann. Entomol. Soc. Am. 60, 1074–1076.Google Scholar
  47. Metcalf, Z.P. (1932–64) General Catalogue of the Hemiptera — Homoptera. US Department of Agriculture, Washington, DC.Google Scholar
  48. Nault, L.R. (1987) Origin and evolution of Auchenorrhyncha-transmitted, plant infecting viruses. In 2nd International Workshop on Leafhoppers and Planthoppers of Economic Importance (M.R. Wilson and L.R. Nault, eds), pp. 131–149, CAB, London.Google Scholar
  49. Newby, R. (1979) Growth and feeding in two species of Machaerotidae (Homoptera). Aust. J. Zool. 27, 395–401.Google Scholar
  50. Nobel, P.S. (1983) Biophysical Plant Physiology and Ecology. W.H. Freeman, San Francisco, CA.Google Scholar
  51. Novotny, V. (1992) Community structure of Auchenorrhyncha (Homoptera) in montane rain forest in Vietnam. J. Trop. Ecol. 8, 169–179.Google Scholar
  52. Novotny, V. (1993) Spatial and temporal components of species diversity in Auchenorrhyncha (Hemiptera) communities of Indochinese montane rain forest. J. Trop. Ecol. 9, 93–100.Google Scholar
  53. Novotny, V. and Kindlmann, P. (1996) Distribution of arthropod body sizes in taxa and communities. Oikos 75, 75–82.Google Scholar
  54. O'Brien, L.B. and Wilson, S.W. (1985) Planthopper systematics and taxonomy. In The Leafhoppers and Planthoppers (L.R. Nault and J.G. Rodriguez, eds), pp. 61–102. Wiley Interscience, New York.Google Scholar
  55. Pagel, M.D. and Harvey, P.H. (1989) Comparative methods for examining adaptation depend on evolutionary models. Folia Primatologica 53, 203–220.Google Scholar
  56. Peters, R.H. (1983) The Ecological Implications of Body Size. Cambridge University Press, Cambridge.Google Scholar
  57. Pollard, D.G. (1968) Stylet penetration and feeding damage of Eupteryx melissae Curtis (Hemiptera, Cicadellidae) on sage. Bull. Entomol. Res. 58, 55–71.Google Scholar
  58. Pollard, D.G. (1972) The stylet structure of a leafhopper (Eupteryx melissae Curtis: Homoptera, Cicadellidae). J. Nat. Hist. 6, 261–271.Google Scholar
  59. Press, M.C. and Whittaker, J.B. (1993) Exploitation of the xylem stream by parasitic organisms. Phil. Trans. R. Soc. Lond. B 341, 101–111.Google Scholar
  60. Raven, J.A. (1983) Phytophages of xylem and phloem: A comparison of animal and plant sapfeeders. Adv. Ecol. Res. 13, 135–234.Google Scholar
  61. Rayner, J.M.V. (1985) Linear relations in biomechanics: The statistics of scaling functions. J. Zool. 206, 415–439.Google Scholar
  62. Rossi, A.M. and Strong, D.R. (1991) Effects of host-plant nitrogen on the preference and performance of laboratory populations of Carneocephala floridana (Homoptera: Cicadellidae). Environ. Entomol. 20, 1349–1355.Google Scholar
  63. Schmidt-Nielsen, K. (1984) Scaling: Why is Animal Size so Important? Cambridge University Press, Cambridge.Google Scholar
  64. Sorensen, J.T., Campbell, B.C., Gill, R.J. and Steffen-Campbell, J.D. (1995) Non-monophyly of Auchenorrhyncha (‘Homoptera’), based upon 18S rDNA phylogeny: Eco-evolutionary and cladistic implications within pre-Heteropterodea Hemiptera (s. 1.) and a proposal for new monophyletic suborders. Pan-Pacific Entomologist 71, 31–60.Google Scholar
  65. Stearns, S.C. (1992) The Evolution of Life Histories. Oxford University Press, Oxford.Google Scholar
  66. Tavella, L. and Arzone, A. (1993) Comparative morphology of mouth parts of Zyginidia pullula, Empoasca vitis, and Graphocephala fennahi (Homoptera, Auchenorrhyncha). Boll. Zool. 60, 33–39.Google Scholar
  67. Terra, W.R. (1990) Evolution of digestive systems of insects. Ann. Rev. Entomol. 35, 181–200.CrossRefGoogle Scholar
  68. Thompson, V. (1994) Spittlebug indicators of nitrogen-fixing plants. Ecol. Entomol. 19, 391–398.Google Scholar
  69. Wasserman, S.S. and Mitter, C. (1978) The relationship of body size to breadth of diet in some Lepidoptera. Ecol. Entomol. 3, 155–160.Google Scholar
  70. Weaver, C.R. and King, D.R. (1954) Meadow spittlebug, Philaenus leucophthalmus (L.). Res. Bull. Ohio Agric. Exp. Stn 741, 1–99.Google Scholar
  71. White, J. and Strehl, C.E. (1978) Xylem feeding by periodical cicada nymphs on tree roots. Ecol. Entomol. 3, 323–327.Google Scholar
  72. Wiegert, R.G. (1964) Population energetics of meadow spittlebugs (Philaenus spumarius L.) as affected by migration and habitat. Ecol. Monogr. 34, 217–241.Google Scholar
  73. Wilson, S.W., Mitter, C., Denno, R.F. and Wilson, M.R. (1994) Evolutionary patterns of host plant use by delphacid planthoppers and their relatives. In Planthoppers: Their Ecology and Management (R.H. Denno and T.J. Perfect, eds), pp. 7–113. Chapman and Hall, New York.Google Scholar
  74. Wood, T.K. (1993) Diversity in the New World Membracidae. Ann. Rev. Entomol. 38, 409–435.CrossRefGoogle Scholar
  75. Young, A.M. (1984) On the evolution of cicada × host-tree associations in Central America. Acta Biotheoretica 33, 163–198.CrossRefGoogle Scholar
  76. Young, D.A. (1968) Taxonomic Study of the Cicadellinae (Homoptera: Cicadellinae). Part 1, Proconiini. Smithsonian Institution Press, Washington, DC.Google Scholar
  77. Young, D.A. (1977) Taxonomic Study of the Cicadellinae (Homoptera: Cicadellinae). Part 2, New World Cicadellini and the Genus Cicadella. North Carolina Experimental Station, Raleigh, NC.Google Scholar
  78. Young, D.A. (1986) Taxonomic Study of the Cicadellinae (Homoptera: Cicadellinae). Part 3, Old World Cicadellini. North Carolina Experimental Station, Raleigh, NC.Google Scholar
  79. Zimmermann, U., Meinzer, F.C., Benkert, R., Zhu, J.J., Schneider, H., Goldstein, G., Kuchenbrod, E. and Haase, A. (1994) Xylem water transport: Is the available evidence consistent with the cohesion theory? Plant, Cell and Environment 17, 1169–1181.Google Scholar
  80. Zrzavy, J. (1992) Evolution of antennae and historical ecology of the hemipteran insects (Paraneoptera). Acta Entomol. Bohemoslov. 89, 77–86.Google Scholar

Copyright information

© Chapman and Hall 1997

Authors and Affiliations

  • Vojtech Novotny
    • 1
  • Michael R. Wilson
    • 2
  1. 1.Institute of Entomology, Czech Academy of Sciences and Faculty of Biological SciencesUniversity of South BohemiaCeske BudejoviceCzech Republic
  2. 2.Department of ZoologyNational Museum of WalesCardiffUK

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