Skip to main content
SpringerLink
Log in

Lagged effects of early-season herbivores on valley oak fecundity

  • Population ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The seasonal match between folivore and leaf phenology affects the annual success of arboreal folivore populations because many folivores exploit developing leaves, which are an ephemeral resource. One strategy for folivores to exploit early-season leaves is to anticipate their emergence. The consequence of this behavior for trees is that individuals that set leaves earlier may experience greater rates of folivore damage, with potential negative fitness consequences. To test this hypothesis, we surveyed the early-season phenology, insect folivore damage, and acorn crop of a population of valley oaks (Quercus lobata) over a 3-year period. We found that trees that set leaves earlier experienced greater rates of folivore damage than trees that set leaves later in the season. In addition, we observed a lagged effect of folivore damage on acorn production, whereby trees with greater leaf damage produced fewer acorns in the subsequent year. These results indicate potential negative fitness consequences of earlier leaf phenology. Our study suggests that folivore pressure may be one factor that affects the optimal timing of leaf set in oaks.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aide TM (1993) Patterns of leaf development and herbivory in a tropical understory community. Ecology 74:455–466

    Article  Google Scholar 

  • Augspurger CK (1981) Reproductive synchrony of a tropical shrub: experimental studies on effects of pollinators and seed predators on Hybanthus prunifolius (Violaceae). Ecology 62:775–788

    Article  Google Scholar 

  • Augspurger CK (2009) Spring 2007 warmth and frost: phenology, damage and refoliation in a temperate deciduous forest. Funct Ecol 23:1031–1039

    Article  Google Scholar 

  • Augspurger CK (2011) Frost damage and its cascading negative effects on Aesculus glabra. Plant Ecol 212:1193–1203

    Article  Google Scholar 

  • Barringer BC, Koenig WD, Knops JMH (2013) Interrelationships among life-history traits in three California oaks. Oecologia 171:129–139

    Article  PubMed  Google Scholar 

  • Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20:441–448

    Article  PubMed  Google Scholar 

  • Cattelino PJ, Becker CA, Fuller LG (1986) Construction and installation of homemade dendrometer bands. North J Appl For 3:73–75

    Google Scholar 

  • Chen Z, Clancy KM, Kolb TE (2003) Variation in budburst phenology of Douglas-fir related to western spruce budworm (Lepidoptera: tortricidae) fitness. J Econ Entomol 96:377–387

    Article  PubMed  Google Scholar 

  • Crawley MJ (1985) Reduction of oak fecundity by low-density herbivore populations. Nature 314:163–164

    Article  Google Scholar 

  • Crawley MJ, Akhteruzzaman M (1988) Individual variation in the phenology of oak trees and its consequences for herbivorous insects. Funct Ecol 2:409–415

    Article  Google Scholar 

  • Elzinga JA, Atlan A, Biere A, Gigord L, Weis AE, Bernasconi G (2007) Time after time: flowering phenology and biotic interactions. Trends Ecol Evol 22:432–439

    Article  PubMed  Google Scholar 

  • Feeny P (1970) Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51:565–581

    Article  Google Scholar 

  • Forkner RE, Marquis RJ, Lill JT, Le Corff J (2008) Timing is everything? Phenological synchrony and population variability in leaf-chewing herbivores of Quercus. Ecol Entomol 33:276–285

    Article  Google Scholar 

  • Geber MA, Griffen LR (2003) Inheritance and natural selection on functional traits. Int J Plant Sci 164:S21–S42

    Article  Google Scholar 

  • Hunter MD (1992) A variable insect plant interaction: the relationship between tree budburst phenology and population levels of insect herbivores among trees. Ecol Entomol 17:91–95

    Article  Google Scholar 

  • Ichie T, Nakagawa M (2013) Dynamics of mineral nutrient storage for mast reproduction in the tropical emergent tree Dryobalanops aromatica. Ecol Res 28:151–158

    Article  Google Scholar 

  • Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362

    Article  PubMed  Google Scholar 

  • Karban R (2008) Leaf drop in evergreen Ceanothus velutinus as a means of reducing herbivory. Ecology 89:2446–2452

    Article  PubMed  Google Scholar 

  • Knops JMH, Koenig WD, Carmen WJ (2007) Negative correlation does not imply a tradeoff between growth and reproduction in California oaks. Proc Natl Acad Sci USA 104:16982–16985

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Koenig WD, Knops JMH, Carmen WJ, Stanback MT, Mumme RL (1994a) Estimating acorn crops using visual surveys. Can J For Res 24:2105–2112

    Article  Google Scholar 

  • Koenig WD, Mumme RL, Carmen WJ, Stanback MT (1994b) Acorn production by oaks in central coastal California: varaiton within and among years. Ecology 75:99–109

    Article  Google Scholar 

  • Koenig WD, Knops JMH, Carmen WJ, Stanback MT, Mumme RL (1996) Acorn production by oaks in central coastal California: influence of weather at three levels. Can J For Res 26:1677–1683

    Article  Google Scholar 

  • Koenig WD, Funk KA, Kraft TS, Carmen WJ, Barringer BC, Knops JMH (2012) Stabilizing selection for within-season flowering phenology confirms pollen limitation in a wind-pollinated tree. J Ecol 100:758–763

    Article  Google Scholar 

  • Koenig WD, Knops JMH, Carmen WJ, Pearse IS (2015) What drives masting? The phenological synchrony hypothesis. Ecology. doi:10.1890/14-0819.1

  • Marquis RJ, Whelan CJ (1994) Insectivorous birds increase growth of white oak through consumption of leaf-chewing insects. Ecology 75:2007–2014

    Article  Google Scholar 

  • Miyazaki Y (2013) Dynamics of internal carbon resources during masting behavior in trees. Ecol Res 28:143–150

    Article  CAS  Google Scholar 

  • Mopper S, Simberloff D (1995) Differential herbivory in an oak population: the role of plant phenology and insect performance. Ecology 76:1233–1241

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R 2 from generalized mixed-effects models. Method Ecol Evol 4:133–142

    Article  Google Scholar 

  • Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob Chang Biol 13:1860–1872

    Article  Google Scholar 

  • Pearse IS, Hipp AL (2009) Phylogenetic and trait similarity to a native species predict herbivory on non-native oaks. Proc Natl Acad Sci USA 106:18097–18102

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pearse IS, Karban R (2013) Leaf drop affects herbivory in oaks. Oecologia 173:925–932

    Article  PubMed  Google Scholar 

  • Pearse IS, Koenig WD, Knops JMH (2014) Cues vs proximate drivers: testing the mechanism behind masting behavior. Oikos 123:179–184

    Article  Google Scholar 

  • Pearse IS, Baty J, Herrmann D, Sage R, Koenig WD (2015) Leaf phenology mediates provenance differences in herbivore populations on valley oaks in a common garden (unpublished)

  • Pinheiro J, Bates D, Deb Roy S, Sarkar D, The R Core Development Team (2009) nlme: linear and nonlinear mixed effects models. In: R package version 3.1–93

  • Polgar CA, Primack RB (2011) Leaf-out phenology of temperate woody plants: from trees to ecosystems. New Phytol 191:926–941

    Article  PubMed  Google Scholar 

  • Powell JA, Opler PA (2009) Moths of Western North America. University of California Press, Berkeley

    Book  Google Scholar 

  • R Core Development Team (2012) R v. 2.15.1. R: a language and environment for statistical computing. The R foundation for statistical computing, Vienna, Austria http://www.R-project.org

  • Rathcke B, Lacey EP (1985) Phenological patterns of terrestrial plants. Annu Rev Ecol Syst 16:179–214

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Rothrock MA, Sterling WL (1982) Sequential sampling for arthropods of cotton: its advantages over point sampling. Southwest Entomol 7:70–81

    Google Scholar 

  • Sala A, Hopping K, McIntire EJB, Delzon S, Crone EE (2012) Masting in whitebark pine (Pinus albicaulis) depletes stored nutrients. New Phytol 196:189–199

    Article  CAS  PubMed  Google Scholar 

  • Schemske DW (1977) Flowering phenology and seed set in Claytonia virginica (Portulaceae). Bull Torrey Bot Club 104:254–263

    Article  Google Scholar 

  • Singer MC, Parmesan C (2010) Phenological asynchrony between herbivorous insects and their hosts: signal of climate change or pre-existing adaptive strategy? Philos Trans R Soc B Biol Sci 365:3161–3176

    Article  Google Scholar 

  • Sork VL, Bramble J, Sexton O (1993) Ecology of mast-fruiting in three species of North American deciduous oaks. Ecology 74:528–541

    Article  Google Scholar 

  • Tikkanen O-P, Julkunen-Tiitto R (2003) Phenological variation as protection against defoliating insects: the case of Quercus robur and Operophtera brumata. Oecologia 136:244–251

    Article  PubMed  Google Scholar 

  • van Asch M, Visser ME (2007) Phenology of forest caterpillars and their host trees: the importance of synchrony. Annu Rev Entomol 52:37–55

    Article  PubMed  Google Scholar 

  • van Asch M, van Tienderen PH, Holleman LJM, Visser ME (2007) Predicting adaptation of phenology in response to climate change, an insect herbivore example. Glob Chang Biol 13:1596–1604

    Article  Google Scholar 

  • Watt AD, McFarlane AM (1991) Winter moth on Sitka spruce: synchrony of egg hatch and budburst, and its effect on larval survival. Ecol Entomol 16:387–390

    Article  Google Scholar 

  • Yang LH, Rudolf VHW (2010) Phenology, ontogeny and the effects of climate change on the timing of species interactions. Ecol Lett 13:1–10

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Vince Voegeli and the University of California’s Hastings Reservation for support while conducting this study. We thank Brian Barringer and Eric Walters for help collecting data on folivore damage and oak phenology, John DeBenedictis for help in moth identification, and David Zayaand Marshall McMunn for statistical advice. This study was supported by the National Science Foundation (Grant DEB-0816691) and the University of California Integrated Hardwood Range Management Program. Data supporting this article are archived with Dryad (doi:10.5061/dryad.63rv4).

Author information

Authors and Affiliations

  1. Cornell Lab of Ornithology, 159 Sapsucker Woods Road, Ithaca, NY, 14850, USA

    Ian S. Pearse & Walter D. Koenig

  2. The Illinois Natural History Survey, 1816 S. Oak St, Champaign, IL, 61820, USA

    Ian S. Pearse

  3. School of Biological Sciences, University of Nebraska, Lincoln, NE, 68588, USA

    Kyle A. Funk

  4. Department of Biological Sciences, Class of 1978 Life Sciences Center, Dartmouth College, Hanover, NH, 03755, USA

    Thomas S. Kraft

  5. Department of Neurobiology and Behavior, Cornell University, Ithaca, NY, 14853, USA

    Walter D. Koenig

Authors
  1. Ian S. Pearse
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kyle A. Funk
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas S. Kraft
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Walter D. Koenig
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ian S. Pearse.

Additional information

Communicated by Ian Kaplan.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 19 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pearse, I.S., Funk, K.A., Kraft, T.S. et al. Lagged effects of early-season herbivores on valley oak fecundity. Oecologia 178, 361–368 (2015). https://doi.org/10.1007/s00442-014-3193-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-014-3193-2

Keywords

Search

Navigation