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Herbivory modifies conifer phenology: induced amelioration by a specialist folivore

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Abstract

Herbivory by Zeiraphera canadensis Mut. & Free. (Lepidoptera: Tortricidae), an early season folivore of white spruce [ Picea glauca (Moench) Voss], has been associated with a shift in the timing of bud burst by its host during the subsequent year. We tested the hypothesis that a herbivory-induced shift in the phenology of bud development improves the window for colonisation of white spruce buds by Z. canadensis. Feeding on cortical tissue of elongating shoots caused the destruction of apical buds and an interruption of apical dominance in the year following herbivory. White spruce compensated for damage with the activation of dormant buds; mainly at proximal positions along shoots. As a result, half of all active buds on previously damaged branches were located immediately adjacent egg sites (i.e. previous year's bud scales), whereas <10% of active buds on intact shoots were situated there. More than 40% of newly emerged larvae colonised the basal buds of damaged shoots versus just 10% for intact shoots. Previous herbivory also influenced the initiation of bud burst. All buds flushed 2 days earlier on damaged shoots and date of bud burst was inversely correlated to bud density, indicating that short damaged shoots with large numbers of buds were stronger sinks for nutrients required for bud development. Egg hatch was best synchronized with early bursting buds on damaged branches. As a consequence, 89% of first-instar larvae successfully colonised buds on damaged branches while only 55% were successful on undamaged branches. Improved survival of larvae in the year following herbivory was a direct result of the evolved response by white spruce to the interruption of apical dominance. The pattern of herbivory by Z. canadensis may have evolved as a strategy to enhance the quality of white spruce for their offspring.

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References

  • Aarssen LW, Irwin DL (1991) What selection: herbivory or competition? Oikos 60:261–262

    Google Scholar 

  • Batzer HO (1973) Defoliation by the spruce budworm stimulates epicormic shoots on balsam fir. Environ Entomol 2:727–728

    Google Scholar 

  • Belsky AJ, Carson WP, Jensen CL, Fox GA (1993) Overcompensation by plants: herbivore optimization or red herring? Evol Ecol 7:109–121

    Google Scholar 

  • Cannell MGR, Thompson S, Lines R (1976) An analysis of inherent differences in shoot growth within some north temperate conifers. In: Cannell MGR, Last FT (eds) Tree physiology and yield improvement. Academic Press, London, pp 173–205

  • Carroll AL (1999) Physiological adaptation to temporal variation in conifer foliage by a caterpillar. Can Entomol 131:659–669

    Google Scholar 

  • Carroll AL, Quiring DT (1993) Influence of feeding by Zeiraphera canadensis (Lepidoptera: Tortricidae) on growth of white spruce: Larval density—damage and damage—shoot production relationships. J Appl Ecol 30:629–639

    Google Scholar 

  • Carroll AL, Quiring DT (1994) Intra-tree variation in foliage development influences the foraging strategy of a caterpillar. Ecology 75:1978–1990

    Google Scholar 

  • Carroll AL, Lawlor MF, Quiring DT (1993) Influence of feeding by Zeiraphera canadensis, the spruce bud moth, on stem-wood growth of white spruce. For Ecol Manage 58:41–49

    Google Scholar 

  • Crabbé J, Barnola P (1996) A new conceptual approach to bud dormancy in woody plants. In: Lang GA (ed) Plant dormancy: physiology, biochemistry and molecular biology. CAB International, Wallingford, pp 83–114

    Google Scholar 

  • Ericsson A, Hellqvist C, Långström B, Larsson S, Tenow O (1985) Effects on growth of simulated and induced shoot pruning by Tomicus piniperda as related to carbohydrate and nitrogen dynamics in Scots pine. J Appl Ecol 22:105–124

    Google Scholar 

  • Haukioja E (1990) Induction of defenses in trees. Annu Rev Entomol 36:25–42

    Google Scholar 

  • Haukioja E, Honkanen T (1996) Why are tree responses to herbivory so variable? In: Mattson WJ, Niemelä P, Rousi M (eds) Dynamics of forest herbivory: quest for pattern and principle. USDA For Serv Gen Tech Rep NC-183, North Cent For Exp Sta, St. Paul, Minnesota, pp 1–10

    Google Scholar 

  • Haukioja E, Suomela J, Neuvonen S (1985) Long-term inducible resistance in birch foliage: triggering cues and efficacy on a defoliator. Oecologia 65:363–369

    Google Scholar 

  • Heichel GH, Turner NC (1976) Phenology and leaf growth of defoliated hardwood trees. In: Anderson JF, Kaya HK (eds) Perspectives in forest entomology. Academic Press, London, pp 31–40

  • Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335

    Google Scholar 

  • Honkanen T, Haukioja E (1994) Why does a branch suffer more after branch-wide than after tree-wide defoliation? Oikos 71:441–450

    Google Scholar 

  • Honkanen T, Haukioja E, Suomela J (1994) Effects of simulated defoliation and debudding on needle and shoot growth in Scots pine ( Pinus sylvestris): implications of plant source/sink relationships for plant-herbivore studies. Funct Ecol 8:631–639

    Google Scholar 

  • Hunter AF, Lechowicz MS (1992) Foliage quality changes during canopy development of some northern hardwood trees. Oecologia 89:316–323

    Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago

  • Kozlowski TT (1971) Growth and development of trees. Academic Press, New York

  • Kramer PJ, Kozlowski TT (1979) Physiology of woody plants. Academic Press, New York

  • Larson KC, Whitham TG (1997) Competition between gall aphids and natural plant sinks: plant architecture affects resistance to galling. Oecologia 109:575–582

    Article  Google Scholar 

  • Lawrence RK, Mattson WJ, Haack RA (1997) White spruce and the spruce budworm: defining the phenological window of susceptibility. Can Entomol 129:291–318

    Google Scholar 

  • Lehtilä K (2000) Modelling compensatory regrowth with bud dormancy and gradual activation of buds. Evol Ecol 14:315–330

    Article  Google Scholar 

  • Martin GC (1987) Apical dominance. HortScience 22:824–833

    CAS  Google Scholar 

  • Maschinski J, Whitham TG (1989) The continuum of plant responses to herbivory: the influence of plant association, nutrient availability and timing. Am Nat 134:1-19

    Article  Google Scholar 

  • Mopper S, Maschinski J, Cobb N, Whitham TG (1991) A new look at habitat structure: consequences of herbivore-modified plant architecture. In: Bell S, McCoy ED, Mushinsky HR (eds) Habitat structure. Chapman and Hall, London, pp 260–280

  • Nilsson P, Tuomi J, Åström M (1996) Bud dormancy as a bet-hedging strategy. Am Nat 147:269–281

    Article  Google Scholar 

  • Ostaff DP, Quiring DT (1994) Seasonal distribution of adult eclosion, oviposition, and parasitism and predation of eggs of the spruce bud moth, Zeiraphera canadensis (Lepidoptera: Tortricidae). Can Entomol 126:995–1006

    Google Scholar 

  • Ostaff DP, Quiring DT (2000a) Role of the host plant in the decline of populations of a specialist herbivore, the spruce bud moth. J Anim Ecol 69:263–273

    Article  Google Scholar 

  • Ostaff DP, Quiring DT (2000b) Population trends of a specialist herbivore, the spruce bud moth, in young white spruce stands. Can Entomol 132:825–842

    Google Scholar 

  • Owens JN, Molder M, Langer H (1977) Bud development in Picea glauca. I. Annual growth cycle of vegetative buds and shoot elongation as they relate to date and temperature sums. Can J Bot 55:2728–2745

    Google Scholar 

  • Piene H (1989) Spruce budworm defoliation and growth loss in young balsam fir: recovery of growth in spaced stands. Can J For Res 19:1616–1624

    Google Scholar 

  • Piene H (1991) The sensitivity of young white spruce to spruce budworm defoliation. North J Appl For 8:168–171

    Google Scholar 

  • Phillips IDJ (1975) Apical dominance. Annu Rev Plant Physiol 26:341–367

    Google Scholar 

  • Pollard DFW, Logan KT (1974) The role of tree growth in the differentiation of provenances of black spruce, Picea mariana (Mill.) B.S.P. Can J For Res 4:308–311

    Google Scholar 

  • Quiring DT (1992) Rapid change in suitability of white spruce for a specialist herbivore, Zeiraphera canadensis , as function of leaf age. Can J Zool 70:2132–2138

    Google Scholar 

  • Quiring DT (1993) Influence of intra-tree variation in time of bud burst of white spruce on herbivory and the behaviour and survivorship of Zeiraphera canadensis. Ecol Entomol 18:353–364

    Google Scholar 

  • Quiring DT, Butterworth EW (1994) Genotype and environment interact to influence acceptability and suitability of white spruce for a specialist herbivore, Zeiraphera canadensis. Ecol Entomol 19:230–238

    Google Scholar 

  • Quiring DT, McKinnon ML (1999) Why does early-season herbivory affect subsequent budburst? Ecology 80:1724–1735

    Google Scholar 

  • Quiring DT, Turgeon JJ, Simpson D, Smith A (1991) Genetically based differences in susceptibility of white spruce to the spruce bud moth. Can J For Res 21:42–47

    Google Scholar 

  • Raupp MJ, Werren JH, Sadof CS (1988) Effects of short-term phenological changes in leaf suitability on the survivorship, growth, and development of gypsy moth (Lepidoptera: Lymantriidae) larvae. Environ Entomol 17:316–319

    Google Scholar 

  • Rosenthal JP, Kotanen PM (1994) Terrestrial plant tolerance to herbivory. Trends Ecol Evol 9:145–148

    Google Scholar 

  • Rubinstein B, Nagao MA (1976) Lateral bud outgrowth and its control by the apex. Bot Rev 42:83–113

    CAS  Google Scholar 

  • SPLUS (2001) Guide to statistics, vol 1. Data Analysis Products Division, Mathsoft, Seattle, Wash.

  • Stowe KA, Marquis RJ, Hochwender CG, Simms EL (2000) The evolutionary ecology of tolerance to consumer damage. Annu Rev Ecol Syst 31:565–595

    Google Scholar 

  • Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185

    PubMed  Google Scholar 

  • Trumble JT, Kolodny-Hirsch DM, Ting IP (1993) Plant compensation for arthropod herbivory. Annu Rev Entomol 38:93–119

    Google Scholar 

  • Tuomi JP, Niemelä P, Jussila I, Vuorislao T, Jormalainen V (1989) Delayed budbreak: a defensive response of mountain birch to early-season defoliation? Oikos 54:87–91

    Google Scholar 

  • Tuomi J, Nilsson P, Åström M (1994a) Plant compensatory responses: bud dormancy as an adaptation to herbivory. Ecology 75:1429–1436

    Google Scholar 

  • Tuomi J, Haukioja E, Honkanen T, Augner M (1994b) Potential benefits of herbivore behaviour inducing amelioration of food-plant quality. Oikos 70:161–166

    Google Scholar 

  • Turgeon JJ (1985) Life cycle and behaviour of the spruce budmoth, Zeiraphera canadensis Mut. & Free. (Lepidoptera: Olethreutidae), in New Brunswick. Can Entomol 117:1239–1247

    Google Scholar 

  • Turgeon JJ (1986) The phenological relationship between the larval development of the spruce budmoth, Zeiraphera canadensis (Lepidoptera: Olethreutidae), and white spruce in northern New Brunswick. Can Entomol 118:345–350

    Google Scholar 

  • Whitham TG, Mopper S (1985) Chronic herbivory: impacts on architecture and sex expression of pinyon pine. Science 228:1089–1091

    Google Scholar 

Download references

Acknowledgements

S. Khoury and M. Green provided technical assistance. R. Alfaro, V. Nealis and M. Steinbauer provided critical reviews of an earlier version of this manuscript. S. Magnussen and J. Kershaw provided statistical advice. The cooperation of the Canadian Forest Service and the New Brunswick Department of Natural Resources and Energy is gratefully acknowledged. This study was supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) postgraduate scholarship and a Canadian Forest Service/NSERC supplement to A.L.C., and a NSERC research grant to D.T.Q.

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Correspondence to Allan L. Carroll.

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Carroll, A.L., Quiring, D.T. Herbivory modifies conifer phenology: induced amelioration by a specialist folivore. Oecologia 136, 88–95 (2003). https://doi.org/10.1007/s00442-003-1240-5

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