Advertisement

Oecologia

, Volume 162, Issue 3, pp 673–683 | Cite as

Developmental plasticity and reduced susceptibility to natural enemies following host plant defoliation in a specialized herbivore

  • Glen R. Hood
  • James R. Ott
Plant-Animal interactions - Original Paper

Abstract

Host-specific phytophagous insects that are short lived and reliant on ephemeral plant tissues provide an excellent system in which to investigate the consequences of disruption in the timing of resource availability on consumer populations and their subsequent interactions with higher tropic levels. The specialist herbivore, Belonocnema treatae (Hymenoptera: Cynipidae) induces galls on only newly flushed leaves of live oak, Quercus fusiformis. In central Texas (USA) episodic defoliation of the host creates variation in the timing of resource availability and results in heterogeneous populations of B. treatae that initiate development at different times. We manipulated the timing of leaf flush in live oak via artificial defoliation to test the hypothesis that a 6- to 8-week delay in the availability of resources alters the timing of this gall former’s life cycle events, performance and survivorship on its host, and susceptibility to natural enemies. B. treatae exhibits plasticity in development time, as the interval from egg to emergence was significantly reduced when gallers oviposited into the delayed leaf flush. As a consequence, the phenologies of gall maturation and adult emergence remain synchronized in spite of variation in the timing of resource availability. Per capita gall production and gall-former performance are not significantly affected by the timing of resource availability. The timing of resource availability and natural enemies interact, however, to produce strong effects on survivorship: when exposed to natural enemies, B. treatae developing in galls initiated by delayed oviposition exhibited an order-of-magnitude increase in survivorship. Developmental plasticity allows this gall former to circumvent disruptions in resource availability, maintain synchrony of life cycle events, and results in reduced vulnerability to natural enemies following defoliation of the host plant.

Keywords

Cynipidae Gall former Tri-trophic interactions Phenology 

Notes

Acknowledgments

We thank S. Egan, M. Eubanks, J. Fordyce, C. Nice, and E. Silverfine for reviews of this manuscript, B. Weckerly for statistical advice, and R. Porter and N. Medina for help with fieldwork. The Department of Biology and the College of Science of Texas State University–San Marcos, the Freeman Ranch Advisory Board, and a Theodore Roosevelt Memorial Grant from the American Museum of Natural History provided support to G. Hood. This study complied with the laws and regulations of the United States of America.

References

  1. Askew RR (1971) Parasitic insects, 1st edn. Elsevier, New YorkGoogle Scholar
  2. Barbosa P, Schultz JC (1987) Insect outbreaks, 1st edn. Academic Press, San DeigoGoogle Scholar
  3. Blair CP, Abrahamson WG, Jackman JA, Tyrrell L (2005) Cryptic speciation and host-race formation in a purportedly generalist tumbling flower beetle. Evolution 59:304–316PubMedGoogle Scholar
  4. Briggs CJ, Latto J (1996) The window of vulnerability and its effect on relative parasitoid abundance. Ecol Entomol 21:128–140CrossRefGoogle Scholar
  5. Clancy KM, Price PW (1986) Temporal variation in three-trophic-level interactions among willows, sawflies and parasites. Ecology 67:1601–1607CrossRefGoogle Scholar
  6. Cox DR (1970) The analysis of binary data. Methuen, LondonGoogle Scholar
  7. Craig TP, Itami JK, Price PW (1990) The window of vulnerability of a shoot-galling sawfly to attack by a parasitoid. Ecology 71:1471–1482CrossRefGoogle Scholar
  8. Craig TP, Itami JK, Horner JD (2007) Geographic variation in the evolution and coevolution of a tritrophic interaction. Evolution 61:1137–1152CrossRefPubMedGoogle Scholar
  9. Crawley MJ, Akhteruzzaman M (1988) Individual variation in the phenology of oak trees and its consequence for herbivorous insects. Funct Ecol 2:409–415CrossRefGoogle Scholar
  10. Cryer G (2003) Temporal and spatial patterns of parasitoid attack on a root-galling cynipid. Masters thesis, Department of Biology, Texas State University, San MarcosGoogle Scholar
  11. Cushman JH, Boggs CL, Weiss SB, Murphy DD, Harvey AW, Ehrlich PR (1994) Estimating female reproductive success of a threatened butterfly: influence of emergence time and host plant phenology. Oecologia 99:194–200CrossRefGoogle Scholar
  12. Danks HV (2006) Key themes in the study of seasonal adaptations in insects. II. Life cycle patterns. Appl Entomol Zool 41:1–13CrossRefGoogle Scholar
  13. Denno RF, McClure MS, Ott JR (1995) Competition revisited and resurrected. Annu Rev Entomol 40:297–331CrossRefGoogle Scholar
  14. Drees BM (2004) Oak leaf roller and springtime defoliation of live oak trees. Texas Cooperative Extension E-206Google Scholar
  15. Egan S, Ott JR (2007) Host plant quality and local adaptation determine the distribution of a gall-forming herbivore. Ecology 88:2869–2879CrossRefGoogle Scholar
  16. Eliason EA, Potter DA (2000a) Budburst phenology, plant vigor, and host genotype effects on the leaf-galling generation of Callirhytis cornigera (Hymenoptera: Cynipidae) on pin oak. Environ Entomol 29:1199–1207CrossRefGoogle Scholar
  17. Eliason EA, Potter DA (2000b) Biology of Callirhytis cornigera (Hymenoptera: Cynipidae) and the arthropod community inhabiting its galls. Environ Entomol 29:551–559CrossRefGoogle Scholar
  18. Forkner RE, Marquis RJ, Lill JT, Corff JL (2008) Timing is everything? Phenological synchrony and population variability in leaf-chewing herbivores of Quercus. Ecol Entomol 33:276–285CrossRefGoogle Scholar
  19. Hall MC (2001) Community structure of parasitoids attacking leaf galls of Belonocnema treatae on Quercus fusiformis. Masters thesis, Department of Biology, Texas State University, San MarcosGoogle Scholar
  20. Hayward A, Stone GH (2005) Oak gall wasp communities: evolution and ecology. Basic Appl Ecol 6:435–443CrossRefGoogle Scholar
  21. Hicks BJ, Aegerter JN, Leather SR, Watt AD (2007) Asynchrony in larval development of the pine beauty moth, Panolis flammea, on an introduced host plant may affect parasitoid efficiency. Arthropod Plant Int 1:213–220CrossRefGoogle Scholar
  22. Hood GR (2009) Effects of prior defoliation on the timing of life cycle events and susceptibility to natural enemies of a host specific gall-former. Masters thesis, Department of Biology, Texas State University, San MarcosGoogle Scholar
  23. Horner JD, Craig TP, Itami JK (1999) The influence of oviposition phenology on survival in the host races of Eurosta solidaginis. Entomol Exp Appl 93:121–129CrossRefGoogle Scholar
  24. Joy JB, Crespi BJ (2007) Adaptive radiation of gall-inducing insects within a single host-plant species. Evolution 61:784–795CrossRefPubMedGoogle Scholar
  25. Kaitaniemi P, Ruohomaki K (1999) Effects of autumn temperature and oviposition date on timing of larval development and risk of parasitism in a spring folivore. Oikos 84:435–442CrossRefGoogle Scholar
  26. Kaitaniemi P, Ruohomaki K, Haukioja E (1997) Consequences of defoliation on phenological interaction between Epirrita autumnata and its host plant, mountain birch. Funct Ecol 11:199–208CrossRefGoogle Scholar
  27. Karban R, Baldwin IT (1997) Induced responses to herbivory, 1st edn. University of Chicago, ChicagoGoogle Scholar
  28. Komatsu T, Akimoto S (1995) Genetic differentiation as a result of adaptation to the phenologies of individual host trees in the galling aphid Kaltenbachiella japonica. Ecol Entomol 20:33–42CrossRefGoogle Scholar
  29. Krause SC, Raffa KF (1995) Defoliation intensity and larval age interact to affect sawfly performance of previously injured Pinus resinosa. Oecologia 102:24–30Google Scholar
  30. Lund JN (1998) The biology and ecology of Belonocnema treatae (Hymenoptera: Cynipidae) on its host plant, Quercus fusiformis. Masters thesis, Department of Biology, Texas State University, San MarcosGoogle Scholar
  31. Lund JN, Ott JR, Lyons R (1998) Heterogony in Belonocnema treatae Mayr (Hymenoptera: Cynipidae). Proc Entomol Soc Wash 100:755–763Google Scholar
  32. Mopper S (1996) Adaptive genetic structure in phytophagous insect populations. Trends Ecol Evol 11:235–238CrossRefGoogle Scholar
  33. Mopper S (2005) Phenology—how time creates spatial structure in endophagous insect populations. Ann Zool Fenn 42:327–333Google Scholar
  34. Mopper S, Simberloff D (1995) Differential herbivory in an oak population: the role of plant phenology and insect performance. Ecology 76:1233–1241CrossRefGoogle Scholar
  35. Muller CH (1961) The live oaks of the series Virentes. Am Midl Nat 65:17–39CrossRefGoogle Scholar
  36. Nylin S, Gotthard K (1998) Plasticity in life-history traits. Annu Rev Entomol 43:63–83CrossRefPubMedGoogle Scholar
  37. Ohgushi T (1991) Lifetime fitness and evolution of reproductive pattern in the herbivorous lady beetle. Ecology 72:2110–2122CrossRefGoogle Scholar
  38. Parry D, Herms DA, Mattson WJ (2003) Responses of an insect folivore and its parasitoids to multiyear experimental defoliation of aspen. Ecology 84:1768–1783CrossRefGoogle Scholar
  39. Potter DA, Redmond CT (1989) Early spring defoliation, secondary leaf flush, and leafminer outbreaks on American holly. Oecologia 81:192–197Google Scholar
  40. Price PW, Roininen H, Tahvanainen J (1987) Why does the bud-galling sawfly, Euura mucronata, attack long shoots? Oecologia 74:1–6CrossRefGoogle Scholar
  41. Rehill B, Schultz J (2002) Opposing survivorship and fecundity effects of host phenology on the gall-forming aphid Hormaphis hamamelidis. Ecol Entomol 27:475–483CrossRefGoogle Scholar
  42. Reynolds R (2000) The role of natural enemies in determining the relationship between gall size and emergence success of a host-specific cynipid. Masters thesis, Department of Biology, Texas State University, San MarcosGoogle Scholar
  43. Rieske LK, Raffa KF (1998) Interactions among insect herbivore guilds: influence of thrips bud injury on foliar chemistry and suitability to gypsy moths. J Chem Ecol 24:501–523CrossRefGoogle Scholar
  44. SAS Institute (2007) JMP version 7.0. SAS Institute, Cary, NCGoogle Scholar
  45. Stewart JW, Bailey B (1993) Defoliation of live oak trees by the oak leaf roller and a closely related moth. Texas Agricultural Extension UC-021Google Scholar
  46. Stone GN, Schronrogge K, Atkinson RJ, Bellido D, Pujade-Villar J (2002) The population biology of oak gall wasps (Hymenoptera: Cynipidae). Annu Rev Entomol 47:633–668CrossRefPubMedGoogle Scholar
  47. Tikkanen OP, Julkunen-Tiitto R (2003) Phenological variation as protection against defoliating insects: the case of Quercus robur and Operophtera brumata. Oecologia 136:224–251CrossRefGoogle Scholar
  48. Van Asch M, Visser ME (2007) Phenology of forest caterpillars and their host trees: the importance of synchrony. Annu Rev Entomol 52:37–55CrossRefPubMedGoogle Scholar
  49. Van Dongen S, Backeljau T, Matthysen E, Dhondt AA (1997) Synchronization of hatching date with budburst of individual host (Quercus robur) in the winter moth (Operophtera brumata) and its fitness consequences. J Anim Ecol 66:113–121CrossRefGoogle Scholar
  50. Van Nouhuys S, Lei G (2004) Parasitoid-host metapopulation dynamics: the cause and consequences of phenological asynchrony. J Anim Ecol 73:526–535CrossRefGoogle Scholar
  51. Wallin KF, Raffa KF (2001) Effects of folivory on subcortical plant defenses: can defense theories predict interguild processes? Ecology 82:1387–1400CrossRefGoogle Scholar
  52. Weis AE, Abrahamson WG (1986) Evolution of host-plant manipulation by gall makers: ecological and genetic factors in the Solidago-Eurosta system. Am Nat 127:681–695CrossRefGoogle Scholar
  53. Weis AE, Walton R, Crego CL (1988) Reactive plant tissue sites and population biology of gall makers. Annu Rev Entomol 33:467–486CrossRefGoogle Scholar
  54. Yukawa J (2000) Synchronization of gallers with host plant phenology. Popul Ecol 42:105–113CrossRefGoogle Scholar
  55. Yukawa J, Akimoto K (2006) Influence of synchronization between adult emergence and host plant phenology on the population density of Pseudasphondylia neolitseae (Diptera: Cecidomyiidae) inducing leaf galls on Neolitsea sericea (Lauraceae). Popul Ecol 48:13–21CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of Notre DameNotre DameUSA
  2. 2.Population and Conservation Biology Program, Department of BiologyTexas State University-San MarcosSan MarcosUSA

Personalised recommendations