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.
Similar content being viewed by others
References
Askew RR (1971) Parasitic insects, 1st edn. Elsevier, New York
Barbosa P, Schultz JC (1987) Insect outbreaks, 1st edn. Academic Press, San Deigo
Blair CP, Abrahamson WG, Jackman JA, Tyrrell L (2005) Cryptic speciation and host-race formation in a purportedly generalist tumbling flower beetle. Evolution 59:304–316
Briggs CJ, Latto J (1996) The window of vulnerability and its effect on relative parasitoid abundance. Ecol Entomol 21:128–140
Clancy KM, Price PW (1986) Temporal variation in three-trophic-level interactions among willows, sawflies and parasites. Ecology 67:1601–1607
Cox DR (1970) The analysis of binary data. Methuen, London
Craig TP, Itami JK, Price PW (1990) The window of vulnerability of a shoot-galling sawfly to attack by a parasitoid. Ecology 71:1471–1482
Craig TP, Itami JK, Horner JD (2007) Geographic variation in the evolution and coevolution of a tritrophic interaction. Evolution 61:1137–1152
Crawley MJ, Akhteruzzaman M (1988) Individual variation in the phenology of oak trees and its consequence for herbivorous insects. Funct Ecol 2:409–415
Cryer G (2003) Temporal and spatial patterns of parasitoid attack on a root-galling cynipid. Masters thesis, Department of Biology, Texas State University, San Marcos
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 99:194–200
Danks HV (2006) Key themes in the study of seasonal adaptations in insects. II. Life cycle patterns. Appl Entomol Zool 41:1–13
Denno RF, McClure MS, Ott JR (1995) Competition revisited and resurrected. Annu Rev Entomol 40:297–331
Drees BM (2004) Oak leaf roller and springtime defoliation of live oak trees. Texas Cooperative Extension E-206
Egan S, Ott JR (2007) Host plant quality and local adaptation determine the distribution of a gall-forming herbivore. Ecology 88:2869–2879
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 29:1199–1207
Eliason EA, Potter DA (2000b) Biology of Callirhytis cornigera (Hymenoptera: Cynipidae) and the arthropod community inhabiting its galls. Environ Entomol 29:551–559
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 33:276–285
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 Marcos
Hayward A, Stone GH (2005) Oak gall wasp communities: evolution and ecology. Basic Appl Ecol 6:435–443
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 1:213–220
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 Marcos
Horner JD, Craig TP, Itami JK (1999) The influence of oviposition phenology on survival in the host races of Eurosta solidaginis. Entomol Exp Appl 93:121–129
Joy JB, Crespi BJ (2007) Adaptive radiation of gall-inducing insects within a single host-plant species. Evolution 61:784–795
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 84:435–442
Kaitaniemi P, Ruohomaki K, Haukioja E (1997) Consequences of defoliation on phenological interaction between Epirrita autumnata and its host plant, mountain birch. Funct Ecol 11:199–208
Karban R, Baldwin IT (1997) Induced responses to herbivory, 1st edn. University of Chicago, Chicago
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 20:33–42
Krause SC, Raffa KF (1995) Defoliation intensity and larval age interact to affect sawfly performance of previously injured Pinus resinosa. Oecologia 102:24–30
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 Marcos
Lund JN, Ott JR, Lyons R (1998) Heterogony in Belonocnema treatae Mayr (Hymenoptera: Cynipidae). Proc Entomol Soc Wash 100:755–763
Mopper S (1996) Adaptive genetic structure in phytophagous insect populations. Trends Ecol Evol 11:235–238
Mopper S (2005) Phenology—how time creates spatial structure in endophagous insect populations. Ann Zool Fenn 42:327–333
Mopper S, Simberloff D (1995) Differential herbivory in an oak population: the role of plant phenology and insect performance. Ecology 76:1233–1241
Muller CH (1961) The live oaks of the series Virentes. Am Midl Nat 65:17–39
Nylin S, Gotthard K (1998) Plasticity in life-history traits. Annu Rev Entomol 43:63–83
Ohgushi T (1991) Lifetime fitness and evolution of reproductive pattern in the herbivorous lady beetle. Ecology 72:2110–2122
Parry D, Herms DA, Mattson WJ (2003) Responses of an insect folivore and its parasitoids to multiyear experimental defoliation of aspen. Ecology 84:1768–1783
Potter DA, Redmond CT (1989) Early spring defoliation, secondary leaf flush, and leafminer outbreaks on American holly. Oecologia 81:192–197
Price PW, Roininen H, Tahvanainen J (1987) Why does the bud-galling sawfly, Euura mucronata, attack long shoots? Oecologia 74:1–6
Rehill B, Schultz J (2002) Opposing survivorship and fecundity effects of host phenology on the gall-forming aphid Hormaphis hamamelidis. Ecol Entomol 27:475–483
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 Marcos
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 24:501–523
SAS Institute (2007) JMP version 7.0. SAS Institute, Cary, NC
Stewart JW, Bailey B (1993) Defoliation of live oak trees by the oak leaf roller and a closely related moth. Texas Agricultural Extension UC-021
Stone GN, Schronrogge K, Atkinson RJ, Bellido D, Pujade-Villar J (2002) The population biology of oak gall wasps (Hymenoptera: Cynipidae). Annu Rev Entomol 47:633–668
Tikkanen OP, Julkunen-Tiitto R (2003) Phenological variation as protection against defoliating insects: the case of Quercus robur and Operophtera brumata. Oecologia 136:224–251
Van Asch M, Visser ME (2007) Phenology of forest caterpillars and their host trees: the importance of synchrony. Annu Rev Entomol 52:37–55
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 66:113–121
Van Nouhuys S, Lei G (2004) Parasitoid-host metapopulation dynamics: the cause and consequences of phenological asynchrony. J Anim Ecol 73:526–535
Wallin KF, Raffa KF (2001) Effects of folivory on subcortical plant defenses: can defense theories predict interguild processes? Ecology 82:1387–1400
Weis AE, Abrahamson WG (1986) Evolution of host-plant manipulation by gall makers: ecological and genetic factors in the Solidago-Eurosta system. Am Nat 127:681–695
Weis AE, Walton R, Crego CL (1988) Reactive plant tissue sites and population biology of gall makers. Annu Rev Entomol 33:467–486
Yukawa J (2000) Synchronization of gallers with host plant phenology. Popul Ecol 42:105–113
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 48:13–21
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Thomas Hoffmeister.
Rights and permissions
About this article
Cite this article
Hood, G.R., Ott, J.R. Developmental plasticity and reduced susceptibility to natural enemies following host plant defoliation in a specialized herbivore. Oecologia 162, 673–683 (2010). https://doi.org/10.1007/s00442-009-1492-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-009-1492-9