Eur. J. Entomol. 108 (1): 71-78, 2011 | DOI: 10.14411/eje.2011.009

Comparison of the severity of selection among beech leaves prior to egg-laying between a leaf-mining and two gall-inducing insects

Jean BÉGUINOT
Société d'Histoire Naturelle du Creusot, 12 rue des Pyrénées, F-71200 Le Creusot, France; e-mail: jean-beguinot@orange.fr

 
Quantitative behavioural traits associated with egg-laying, such as the level of selectivity for host-supports and the size of egg clutches, are generally thought to be of great importance for the subsequent survival and development of offspring. These quantitative traits, however, are often difficult to assess reliably by direct observation in the field. This is particularly the case when the insects are very tiny, which is the case for most galling and leaf mining insects. However, a new approach, the "Melba" procedure, allows the indirect inference of these quantitative traits, using easily recorded field-data only. Application of this diagnostic procedure to a large series of samples of beech leaves (Fagus silvatica), harbouring either a leaf miner, Phyllonorycter maestingella (Lepidoptera: Gracillariidae) or one or the other of two galling insects, Mikiola fagi or Hartigiola annulipes (Diptera: Cecidomyiidae) indicates that the leaf miner differs significantly from the two species of galling insect in term of combined values of host-acceptance ratio and average clutch-size, while the two gall-inducing species remain substantially undistinguishable from each other according to these traits. Thus, the galling insects (i) show stronger selectivity for a host than does the miner at any given average clutch-size and (ii) show larger average clutch-size at any given level of selectivity. That is, for at least these three species, the galling insects show a greater level of selectivity when choosing leaves to oviposit on but, then, tend to lay larger egg-clutches. These differences may be due (i) to the gall-inducing process requiring far more of leaf tissues than being simply palatable, which makes it likely that galling species will be more selective in their choice of leaves than leaf miners and (ii) to the capacity of galls to become nutrient sinks, which may help explain why the galling insects laid larger egg clutches. However, whether these trends can be regarded as general rather specific to this particular case, depends on the outcome of future studies on other groups of insects with similar life histories.

Keywords: Behaviour, oviposition, egg-laying, selectivity, host acceptance, clutch size, insect, mine, gall, inference, Lepidoptera, Gracillariidae, Diptera, Cecidomyiidae, Mikiola fagi, Hartigiola annulipes, Phyllonorycter maestingella

Received: February 26, 2010; Accepted: June 25, 2010; Published: January 3, 2011

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References

  1. AUERBACH M. & SIMBERLOFF D. 1989: Oviposition site preference and larval mortality in a leaf-mining moth. Ecol. Entomol. 14: 131-140 Go to original source...
  2. AWMACK C.S. & LEATHER S.R. 2002: Host-plant quality and fecundity in herbivorous insects. Annu. Rev. Entomol. 47: 817-844 Go to original source...
  3. BEGUINOT J. 2005: Comparing the mothers selectivity for leaf quality prior to oviposition in two galling insects (Hymenoptera: Cynipidae), using a new methodological approach for behaviour analysis. Mem. Soc. Hist. Nat. Creusot 1: 1-14
  4. BEGUINOT J. 2008: Quantitative assessment of egg-laying behavioural parameters in insects: refining the original "Melba" procedure to cope with non-integer values of the average clutch-size. Mem. Soc. Hist. Nat. Creusot 4: 37-46
  5. BEGUINOT J. 2009a: The remarkably low leaf-selectivity prior to oviposition in the moth-pest Cameraria ohridella is not unique to this species within the genus Cameraria. Rev. Ecol. (Terre & Vie) 64: 333-341
  6. BEGUINOT J. 2009b: Comparing the ratios of leaf-acceptance prior to egg-laying among several species of leaf-mining moths upon Quercus sp. pl. (Lepidoptera: Gracillariidae, Tischeriidae). Entomol. Gener. 32: 145-154
  7. BERENBAUM M. 1981: Patterns of furanocoumarin distribution and insect herbivory in the Umbelliferae-plant chemistry and community structure. Ecology 62: 1254-1266 Go to original source...
  8. BREWER A.M. & GASTON K.J. 2003: The geographical range structure of the holly leaf-miner. II. Demographic rates. J. Anim. Ecol. 72: 82-93 Go to original source...
  9. BURNSTEIN & WOOL D. 1993: Gall aphids do not select optimal galling sites (Smynthurodes betae; Pemphigidae). Ecol. Entomol. 18: 155-164 Go to original source...
  10. CARRIERE Y. 1998: Constraints on the evolution of host choice by phytophagous insects. Oikos 82: 401-406 Go to original source...
  11. COPE J.M. & FOX J.W. 2003: Oviposition decision in the seed beetle Callosobruchus maculatus (Coleoptera: Bruchidae): effects of seed size on superparasitism. J. Stor. Prod. Res. 39: 355-365 Go to original source...
  12. CORNELISSEN T. & STILING P. 2006: Clumped distribution of oak leaf miners between and within plants. Basic Appl. Ecol. 9: 67-77 Go to original source...
  13. CRAIG T.P., ITAMI J.K. & PRICE P.W. 1986: Resource regulation by a stem-galling sawfly on the arroyo willow. Ecology 67: 419-425 Go to original source...
  14. DAJOZ R. 1981: Lois de distribution de galles de dipteres sur les feuilles du Hetre. Cah. Nat. Bull. N.P. (n.s.) 37: 75-79
  15. DAJOZ R. 1993: Quelques aspects des relations plantes-insectes; leur importance dans la dynamique des populations d'insectes phytophages. Cah. Nat. Bull N.P. (n.s.) 48: 87-103
  16. FAETH S.H. 1991: Novel aspects of host tree resistance to leaf miners. In Baranchikov Y.N., Mattson W.J., Hain F.P. & Payne T.L.: Forest Insects Guilds: Patterns of Interaction with Host Trees. U.S.D.A. Forest Service, Gen. Tech. Rep. NE-153, pp. 219-239
  17. FERNANDES G.W., PRICE P.W., GONCALVES-ALVIM S.J., CRAIG T.P. & YANEGA D. 2000: Response of the galling insect Aciurina trixa Curran (Diptera: Tephritidae) to host plant quality. Ann. Soc. Entomol. Brasil 29: 423-431 Go to original source...
  18. FOX C.W. & CZESAK M.E. 2002: Evolutionary ecology of progeny size in arthropods. Annu. Rev. Entomol. 45: 341-369 Go to original source...
  19. FRY H.R.C., QUIRING D.T., RYALL K.L. & DIXON P.L. 2009: Influence of intra-tree variation in phenology and oviposition site on the distribution and performance of Ennomos subsignaria on mature sycamore maple. Ecol. Entomol. 34: 394-405 Go to original source...
  20. GIBBS M., LACE L.A., JONES M.J. & MOORE A.J. 2005: Egg sizenumber trade-off and a decline in oviposition site choice quality: female Pararge aegeria butterflies pay a cost of having males present at oviposition. J. Insect Sci. 5: 39-48 Go to original source...
  21. GRIPENBERG S. 2007: Spatial Ecology of a Specialist Insect Herbivore - the Leaf-mining Moth Tischeria ekebladella on the Pedunculate Oak Quercus robur. Thesis, University of Helsinki
  22. GRIPENBERG S. & ROSLIN T. 2005: Host plants as islands: resource quality and spatial setting as determinant of insect distribution. Ann. Zool. Fenn. 42: 335-345
  23. GRIPENBERG S. & ROSLIN T. 2007: Up or down in space? Uniting the bottom-up and top-down paradigm and spatial ecology. Oikos 116: 181-188 Go to original source...
  24. GRIPENBERG S., SALMINEN J.P. & ROSLIN T. 2007a: A tree in the eyes of a moth - temporal variation in oak leaf quality and leaf-miner performance. Oikos 116: 592-600
  25. GRIPENBERG S., MORRIEN E., CUDMORE A., SALMINEN J.P. & ROSLIN T. 2007b: Resource selection by female moths in a heterogeneous environment: what is a poor girl to do? J. Anim. Ecol. 76: 854-865 Go to original source...
  26. HEIMPEL G.E. & ROSENHEIM J.A. 1995: Dynamic host feeding by the parasitoid Aphytis melinus: the balance between current and future reproduction. J. Anim. Ecol. 64: 153-167 Go to original source...
  27. JOLIVET P. 1983: Insectes et plantes: Evolution parallele et adaptation. Bull. Soc. Linn. Lyon (Suppl.) 52: 164 pp
  28. KAGATA H. & OHGUSHI T. 2002: Effects of multiple oviposition on clutch size in a leaf-mining moth, Paraleucoptera sinuella (Lepidoptera: Lyonetiidae). Entomol. Sci. 5: 407-410
  29. KOZLOV M.V. & KORICHEVA Y.G. 1991: The within-tree distribution of caterpillar mines. In Baranchikov Y.N., Mattson W.J., Hain F.P. & Payne T.L.: Forest Insects Guilds: Patterns of Interaction with Host Trees. U.S.D.A. Forest Service, Gen. Tech. Rep. NE-153, pp. 240-255
  30. LARRSON S. & EKBOM B. 1995: Oviposition mistakes in herbivorous insects: confusion or a step towards new host plant? Oikos 72: 155-160 Go to original source...
  31. MAYHEW P.J. 1997: Adaptative patterns of host-plant selection by phytophagous insects. Oikos 79: 417-428 Go to original source...
  32. MAYHEW P.J. 2001: Herbivore host choice and optimal bad motherhood. Trends Ecol. Evol. 16: 165-167 Go to original source...
  33. MORRISON A. & QUIRING D. 2009: Intra-plant heterogeneity influences the preference and performance of juveniles and adults of a gall midge. Ecol. Entomol. 34: 287-295 Go to original source...
  34. OBERMAIER E., HEISSWOLF A., POETHKE H.J., RANDLKOFER B. & MEINERS T. 2008: Plant architecture and vegetation structure: two ways for insect herbivores to escape parasitism. Eur. J. Entomol. 105: 233-240 Go to original source...
  35. REALE D. & ROFF D.A. 1992: Quantitative genetics of oviposition behaviour and interactions among oviposition traits in the sand cricket. Anim. Behav. 64: 397-406 Go to original source...
  36. ROSLIN T., GRIPENBERG S., SALMINEN J.P., KARONEN M., O'HARA R.B., PIHLAJA K. & PULKKINEN P. 2006: Seeing the trees for the leaves: oaks as mosaics for a host-specific moth. Oikos 113: 106-120 Go to original source...
  37. SARFRAZ R.N., DOSDALL L.M. & KEDDIE A.B. 2009: Bottom-up effects of host plant nutritional quality on Plutella xylostella (Lepidoptera: Plutellidae) and top-down effects of herbivore attack on plant compensatory ability. Eur. J. Entomol. 106: 583-594 Go to original source...
  38. STEIN S.J. & PRICE P.W. 1995: Relative effects of plant resistance and natural enemies by plant development age on sawfly (Hymenoptera: Tenthredinidae) preference and performance. Environ. Entomol. 24: 909-916 Go to original source...
  39. SUOMELA J. & AYRES M.P. 1994: Within tree and among-tree variation in leaf characteristics of mountain birch and its implications for herbivory. Oikos 70: 212-222 Go to original source...
  40. THOMPSON J.N. & PELLMYR O. 1991: Evolution of oviposition behaviour and host preference in Lepidoptera. Annu. Rev. Entomol. 36: 65-89 Go to original source...
  41. TRAGER M.D., BOYD B.M., DANIELS J.C. & PENCE J.A. 2009: Host plant selection, larval survival and reproductive phenology in Megathymus yuccae (Lepidoptera: Hesperiidae). Environ. Entomol. 38: 1211-1218 Go to original source...
  42. VUORISALO T., WALLS M., NIEMELA P. & KUITUNENE H. 1989: Factors affecting mosaic distribution of galls of an eriophyid mite, Eriophyes laevis, in alder, Alnus glutinosa. Oikos 55: 370-374 Go to original source...
  43. WALLIN K.F. & RAFFA K.F. 1998: Association of within-tree jack pine budworm feeding patterns with canopy level and within needle variation of water, nutrient and monoterpene concentration. Can. J. Forest Res. 28: 228-233 Go to original source...
  44. ZEHNDER C.B., STODOLA K.W., JOYCE B.L., EGETTER D., COOPER R.J. & HUNTER M.D. 2009: Elevational and seasonal variation in the foliar quality and arthropod community of Acer pensylvanicum. Environ. Entomol. 38: 1161-1167 Go to original source...