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

Evolutionary Ecology volume 11, pages 419–437 (1997)Cite this 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.

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References

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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 

  • Backus, E.A. (1988) Sensory systems and behaviours which mediate hemipteran plant-feeding: A taxonomic overview. J. Insect Physiol. 3, 151–165.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • Calder, W.A. III (1984) Size, Function, and Life History. Harvard University Press, Cambridge, MA.

    Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  Google Scholar 

  • Distant, W.L. (1906) The Fauna of British India Including Ceylon and Burma: Rhynchota — Vol. 3. Heteroptera — Homoptera. Taylor and Francis, London.

    Google Scholar 

  • Distant, W.L. (1908) The Fauna of British India Including Ceylon and Burma: Rhynchota — Vol. 4. Homoptera: Appendix. Taylor and Francis, London.

    Google Scholar 

  • Distant, W.L. (1916) The Fauna of British India Including Ceylon and Burma: Rhynchota — Vol. 6. Homoptera: Appendix. Taylor and Francis, London.

    Google Scholar 

  • 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 

  • 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 

  • Dixon, A.F.G. and Kindlmann, P. (submitted) Cost of flight apparatus and optimum body size in insect migrants. Ecology.

  • 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 

  • 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 

  • Field, C.B. and Holbrook, N.M. (1989) Catastrophic xylem failure: Tree life at the brink. TREE 4, 124–126.

    Google Scholar 

  • 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 

  • Gaston, K. J. (1991) Body size and probability of description: The beetle fauna of Britain. Ecol. Entomol. 16, 505–508.

    Google Scholar 

  • 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 

  • Gunthardt, M.S. and Wanner, H. (1981) The feeding behaviour of two leafhoppers on Vicia faba. Ecol. Entomol. 6, 17–22.

    Google Scholar 

  • Hamilton, K.G.A. (1981) Morphology and evolution of the rhynchotan head (Insecta: Hemiptera, Homoptera). Can. Entomol. 113, 953–974.

    Google Scholar 

  • Hamilton, K.G.A. (1982) The Spittlebugs of Canada. Homoptera: Cercopidae. Canadian Government Publishing Centre, Ottawa.

    Google Scholar 

  • 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 

  • Hanken, J. and Wake, D.B. (1993) Miniaturization of body size: Organismal consequences and evolutionary significance. Ann. Rev. Ecol. Syst. 24, 501–519.

    Article  Google Scholar 

  • Harvey, P.M. and Pagel, M.D. (1991) The Comparative Method in Evolutionary Biology. Oxford University Press, New York.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • Horsfield, D. (1978) Evidence for xylem feeding by Philaenus spumarius (L.) (Homoptera: Cercopidae). Entomol. Exp. Appl. 24, 95–99.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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 

  • La Barbera, M. (1989) Analyzing body size as a factor in ecology and evolution. Ann. Rev. Ecol. Syst. 20, 97–117.

    Article  Google Scholar 

  • Lindstrom, J., Kaila, L. and Niemela, P. (1994) Polyphagy and adult body size in geometrid moths. Oecologia 98, 130–132.

    Article  Google Scholar 

  • 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 

  • Mattson, W.J. (1980) Herbivory in relation to plant nitrogen content. Ann. Rev. Ecol. Syst. 11, 119–161.

    Article  Google Scholar 

  • McKitrick, M.C. (1993) Phylogenetic constraint in evolutionary theory: Has it any explanatory power? Ann. Rev. Ecol. Syst. 24, 307–330.

    Article  Google Scholar 

  • Mittler, T.E. (1967) Water tension in plants — an entomological approach. Ann. Entomol. Soc. Am. 60, 1074–1076.

    Google Scholar 

  • Metcalf, Z.P. (1932–64) General Catalogue of the Hemiptera — Homoptera. US Department of Agriculture, Washington, DC.

    Google Scholar 

  • 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 

  • Newby, R. (1979) Growth and feeding in two species of Machaerotidae (Homoptera). Aust. J. Zool. 27, 395–401.

    Google Scholar 

  • Nobel, P.S. (1983) Biophysical Plant Physiology and Ecology. W.H. Freeman, San Francisco, CA.

    Google Scholar 

  • Novotny, V. (1992) Community structure of Auchenorrhyncha (Homoptera) in montane rain forest in Vietnam. J. Trop. Ecol. 8, 169–179.

    Google Scholar 

  • 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 

  • Novotny, V. and Kindlmann, P. (1996) Distribution of arthropod body sizes in taxa and communities. Oikos 75, 75–82.

    Google Scholar 

  • 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 

  • Pagel, M.D. and Harvey, P.H. (1989) Comparative methods for examining adaptation depend on evolutionary models. Folia Primatologica 53, 203–220.

    Google Scholar 

  • Peters, R.H. (1983) The Ecological Implications of Body Size. Cambridge University Press, Cambridge.

    Google Scholar 

  • 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 

  • Pollard, D.G. (1972) The stylet structure of a leafhopper (Eupteryx melissae Curtis: Homoptera, Cicadellidae). J. Nat. Hist. 6, 261–271.

    Google Scholar 

  • 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 

  • Raven, J.A. (1983) Phytophages of xylem and phloem: A comparison of animal and plant sapfeeders. Adv. Ecol. Res. 13, 135–234.

    Google Scholar 

  • Rayner, J.M.V. (1985) Linear relations in biomechanics: The statistics of scaling functions. J. Zool. 206, 415–439.

    Google Scholar 

  • 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 

  • Schmidt-Nielsen, K. (1984) Scaling: Why is Animal Size so Important? Cambridge University Press, Cambridge.

    Google Scholar 

  • 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 

  • Stearns, S.C. (1992) The Evolution of Life Histories. Oxford University Press, Oxford.

    Google Scholar 

  • 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 

  • Terra, W.R. (1990) Evolution of digestive systems of insects. Ann. Rev. Entomol. 35, 181–200.

    Article  Google Scholar 

  • Thompson, V. (1994) Spittlebug indicators of nitrogen-fixing plants. Ecol. Entomol. 19, 391–398.

    Google Scholar 

  • 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 

  • Weaver, C.R. and King, D.R. (1954) Meadow spittlebug, Philaenus leucophthalmus (L.). Res. Bull. Ohio Agric. Exp. Stn 741, 1–99.

    Google Scholar 

  • White, J. and Strehl, C.E. (1978) Xylem feeding by periodical cicada nymphs on tree roots. Ecol. Entomol. 3, 323–327.

    Google Scholar 

  • 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 

  • 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 

  • Wood, T.K. (1993) Diversity in the New World Membracidae. Ann. Rev. Entomol. 38, 409–435.

    Article  Google Scholar 

  • Young, A.M. (1984) On the evolution of cicada × host-tree associations in Central America. Acta Biotheoretica 33, 163–198.

    Article  Google Scholar 

  • Young, D.A. (1968) Taxonomic Study of the Cicadellinae (Homoptera: Cicadellinae). Part 1, Proconiini. Smithsonian Institution Press, Washington, DC.

    Google Scholar 

  • 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 

  • Young, D.A. (1986) Taxonomic Study of the Cicadellinae (Homoptera: Cicadellinae). Part 3, Old World Cicadellini. North Carolina Experimental Station, Raleigh, NC.

    Google Scholar 

  • 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 

  • Zrzavy, J. (1992) Evolution of antennae and historical ecology of the hemipteran insects (Paraneoptera). Acta Entomol. Bohemoslov. 89, 77–86.

    Google Scholar 

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  1. Institute of Entomology, Czech Academy of Sciences and Faculty of Biological Sciences, University of South Bohemia, Branisovska 31, 370 05, Ceske Budejovice, Czech Republic

    Vojtech Novotny

  2. Department of Zoology, National Museum of Wales, Cathays Park, Cardiff, CF1 3NP, UK

    Michael R. Wilson

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Novotny, V., Wilson, M.R. Why are there no small species among xylem-sucking insects?. Evolutionary Ecology 11, 419–437 (1997). https://doi.org/10.1023/A:1018432807165

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  • DOI: https://doi.org/10.1023/A:1018432807165

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