Skip to main content

Advertisement

Log in

Seed predation and climate impacts on reproductive variation in temperate forests of the southeastern USA

  • Global change ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Climatic effects on tree recruitment will be determined by the interactive effects of fecundity and seed predation. Evaluating how insect and vertebrate seed predators mediate tree reproductive responses to climate depends on long-term studies of seed production, development, and predation. In this study, our objectives were to (1) assess the effects of interannual climate variation on seed abortion rates, (2) assess the impact of seed density on predation rates, and (3) examine the degree to which density-dependent seed predation would amplify or dampen interannual variation in fecundity associated with seed abortion. We used a 19-year study of seed abortion and pre-dispersal predation rates by insects and vertebrates (birds and rodents) for five temperate tree species across forest plots from the North Carolina Piedmont to the Southern Appalachian Mountains in the southeastern USA. We found that rates of seed abortion and predation increased reproductive variation for oaks (Quercus species). Probability of seed abortion was greatest during years with cool, dry springs. Responses of seed predation on Quercus species to current year’s seed density varied by species, but exhibited positive density-dependence to previous year’s seed density consistent with numerical responses of seed predators. Seed abortion and predation rates for two drupe species responded little to variation in climate or seed density, respectively. Given that predation increased interannual variation in seed availability and the negative density-dependence to previous year’s seed density, our results indicate that consistent numerical responses of oak seed predators may amplify interannual variation due to climate-mediated processes like seed abortion.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Allen RB, Mason NWH, Richardson SJ, Platt KH (2011) Synchronicity, periodicity and bimodality in inter-annual tree seed production along an elevation gradient. Oikos 121:367–376

    Article  Google Scholar 

  • Beal JA, Haliburton W, Knight FB (1952) Forest insects of the southeast: with special reference to species occurring in the Piedmont Plateau of North Carolina. Duke University School of Forestry Bulletin 14

  • Buonaccorsi JP, Elkinton J, Koenig W et al (2003) Measuring mast seeding behavior: relationships among population variation, individual variation and synchrony. J Theor Biol 224:107–114

    Article  PubMed  Google Scholar 

  • Burns RM, Honkala BH (1990) Silvics of North America. Volume 1. Conifers. Agriculture Handbook, Washington, No. 654, pp 675

  • Cecich RA, Sullivan NH (1999) Influence of weather at time of pollination on acorn production of Quercus alba and Quercus velutina. Can J For Res 29:1817–1823

    Article  Google Scholar 

  • Clark JS, Macklin E, Wood L (1998) Stages and spatial scales of recruitment limitation in southern Appalachian forests. Ecol Monogr 68:213–235

    Article  Google Scholar 

  • Clark JS, Beckage B, Camill P et al (1999) Interpreting recruitment limitation in forests. Am J Bot 86:1–16

    Article  CAS  PubMed  Google Scholar 

  • Clark JS, Bell D, Chu C et al (2010) High-dimensional coexistence based on individual variation: a synthesis of evidence. Ecol Appl 80:569–608

    Google Scholar 

  • Clark JS, Bell DM, Hersh MH, Nichols L (2011) Climate change vulnerability of forest biodiversity: climate and competition tracking of demographic rates. Glob Change Biol 17:1834–1849

    Article  Google Scholar 

  • Clark JS, Bell DM, Kwit M et al (2012) Individual-scale inference to anticipate climate-change vulnerability of biodiversity. Philos Trans R Soc B 367:236–246

    Article  Google Scholar 

  • Crone EE, McIntire EJB, Brodie J (2011) What defines mast seeding? Spatio-temporal patterns of cone production by whitebark pine. J Ecol 99:438–444

    Google Scholar 

  • Espelta JM, Cortés P, Molowny-Horas R et al (2008) Masting mediated by summer drought reduces acorn predation in Mediterranean oak forests. Ecology 89:805–817

    Article  PubMed  Google Scholar 

  • Espelta JM, Bonal R, Sánchez-Humanes B (2009) Pre-dispersal acorn predation in mixed oak forests: interspecific differences are driven by the interplay among seed phenology, seed size and predator size. J Ecol 97:1416–1423

    Article  Google Scholar 

  • Gelfand AE, Ghosh SK (1998) Model choice: a minimum posterior predictive loss approach. Biometrika 85:1–11

    Article  Google Scholar 

  • Govindan BN, Kéry M, Swihart RK (2011) Host selection and responses to forest fragmentation in acorn weevils: inferences from dynamic occupancy models. Oikos 121:623–633

    Article  Google Scholar 

  • Herrera CM, Jordano P, Guitián J, Traveset A (1998) Annual variability in seed production by woody plants and the masting concept: reassessment of principles and relationship to pollination and seed dispersal. Am Nat 152:576–594

    Article  CAS  PubMed  Google Scholar 

  • Houle G (1999) Mast seeding in Abies balsamea, Acer saccharum and Betula alleghaniensis in an old growth, cold temperate forest of north-eastern North America. J Ecol 87:413–422

    Article  Google Scholar 

  • Howe HF (1989) Scatter-and clump-dispersal and seedling demography: hypothesis and implications. Oecologia 79:417–426

    Article  CAS  PubMed  Google Scholar 

  • Hughes J, Vogler AP (2004) Ecomorphological adaptation of acorn weevils to their oviposition site. Evolution 58:1971–1983

    Article  PubMed  Google Scholar 

  • Ichie T, Igarashi S, Yoshida S et al (2013) Are stored carbohydrates necessary for seed production in temperate deciduous trees? J Ecol 101:525–531

    Article  CAS  Google Scholar 

  • Janzen DH (1971) Seed predation by animals. Annu Rev Ecol Syst 2:475–492

    Article  Google Scholar 

  • Jordano P, García C, Godoy JA, García-Castaño JL (2007) Differential contribution of frugivores to complex seed dispersal patterns. Proc Natl Acad Sci USA 104:3278–3282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelly D (1994) The evolutionary ecology of mast seeding. Trends Ecol Evol 9:465–470

    Article  CAS  PubMed  Google Scholar 

  • Kelly D, Hart DE, Allen RB (2001) Evaluating the wind pollination benefits of mast seeding. Ecology 82:117–126

    Article  Google Scholar 

  • Kelly D, Geldenhuis A, James A et al (2013) Of mast and mean: differential-temperature cue makes mast seeding insensitive to climate change. Ecol Lett 16:90–98

    Article  PubMed  Google Scholar 

  • Keyantash J, Dracup JA (2002) The quantification of drought: an evaluation of drought indices. Bull Am Meteorol Soc 83:1167–1180

    Article  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Koenig W, Knops J (2000) Patterns of annual seed production by northern hemisphere trees: a global perspective. Am Nat 155:59–69

    Article  PubMed  Google Scholar 

  • Koenig WD, Knops JMH (2014) Environmental correlates of acorn production by four species of Minnesota oaks. Popul Ecol 56:63–71

    Article  Google Scholar 

  • Koenig WD, Knops J, Carmen WJ et al (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, Kelly D, Sork VL et al (2003) Dissecting components of population-level variation in seed production and the evolution of masting behavior. Oikos 102:581–591

    Article  Google Scholar 

  • Koenig WD, Knops JMH, Carmen WJ, Pearse IS (2015) What drives masting? The phenological synchrony hypothesis. Ecology 96:184–192

    Article  PubMed  Google Scholar 

  • Lombardo JA, McCarthy BC (2008) Silvicultural treatment effects on oak seed production and predation by acorn weevils in southeastern Ohio. For Ecol Manage 255:2566–2576

    Article  Google Scholar 

  • Lombardo JA, McCarthy BC (2009) Seed germination and seedling vigor of weevil-damaged acorns of red oak. Can J For Res 39:1600–1605

    Article  Google Scholar 

  • Maeto K, Ozaki K (2003) Prolonged diapause of specialist seed-feeders makes predator satiation unstable in masting of Quercus crispula. Oecologia 137:392–398

    Article  PubMed  Google Scholar 

  • Marquis DA, Eckert PL, Roach BA (1976) Acorn weevils, rodents, and deer all contribute to oak-regeneration difficulties in Pennsylvania. Research Paper NE-365, USDA Forest Service Northern Experiment Station, Upper Darby, PA, USA

  • McShea WJ (2000) The influence of acorn crops on annual variation in rodent and bird populations. Ecology 81:228–238

    Article  Google Scholar 

  • Mearns LO, Giorgi F, McDaniel L, Shields C (2003) Climate scenarios for the southeastern US based on GCM and regional model simulations. Clim Change 60:7–35

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Morin X, Augspurger C, Chuine I (2007) Process-based modeling of species“distributions: what limits temperate tree species” range boundaries? Ecology 88:2280–2291

    Article  PubMed  Google Scholar 

  • Mund M, Kutsch WL, Wirth C et al (2010) The influence of climate and fructification on the inter-annual variability of stem growth and net primary productivity in an old-growth, mixed beech forest. Tree Physiol 30:689–704

    Article  CAS  PubMed  Google Scholar 

  • Ostfeld RS, Keesing F (2000) Pulsed resources and community dynamics of consumers in terrestrial ecosystems. Trends Ecol Evol 15:232–237

    Article  PubMed  Google Scholar 

  • Ostfeld RS, Jones CG, Wolff JO (1996) Of mice and mast. BioScience 46:323–330

    Article  Google Scholar 

  • Ostfeld RS, Canham CD, Oggenfuss K et al (2006) Climate, deer, rodents, and acorns as determinants of variation in lyme-disease risk. PLoS Biol 4:e145

    Article  PubMed  PubMed Central  Google Scholar 

  • Pearse IS, Koenig WD, Knops JMH (2013) Cues versus proximate drivers: testing the mechanism behind masting behavior. Oikos 123:179–184

    Article  Google Scholar 

  • Pearse IS, Koenig WD, Funk KA, Pesendorfer MB (2015) Pollen limitation and flower abortion in a wind-pollinated, masting tree. Ecology 96:587–593

    Article  PubMed  Google Scholar 

  • Pérez-Ramos IM, Urbieta IR, Marañón T et al (2008) Seed removal in two coexisting oak species: ecological consequences of seed size, plant cover and seed-drop timing. Oikos 117:1386–1396

    Article  Google Scholar 

  • Pérez-Ramos IM, Ourcival JM, Limousin JM, Rambal S (2010) Mast seeding under increasing drought: results from a long-term data set and from a rainfall exclusion experiment. Ecology 91:3057–3068

    Article  PubMed  Google Scholar 

  • Reid JL, Katsuki KN, Holl KD (2012) Do birds bias measurements of seed rain? J Trop Ecol 28:421–422

    Article  Google Scholar 

  • Sallabanks R, Courtney SP (1992) Frugivory, seed predation, and insect-vertebrate interactions. Annu Rev Entomol 37:377–400

    Article  CAS  PubMed  Google Scholar 

  • Samuels IA, Levey DJ (2005) Effects of gut passage on seed germination: do experiments answer the questions they ask? Funct Ecol 19:365–368

    Article  Google Scholar 

  • Satake A, Bjørnstad ON (2004) Spatial dynamics of specialist seed predators on synchronized and intermittent seed production of host plants. Am Nat 163:591–605

    Article  PubMed  Google Scholar 

  • Satake A, Bjørnstad ON (2007) A resource budget model to explain intraspecific variation in mast reproductive dynamics. Ecol Res 23:3–10

    Article  Google Scholar 

  • Schauber EM, Kelly D, Turchin P et al (2002) Synchronous and asynchronous masting by 18 New Zealand plant species: the role of temperature cues and implications for climate change. Ecology 83:1214–1225

    Article  Google Scholar 

  • Schnurr JL, Ostfeld RS, Canham CD (2002) Direct and indirect effects of masting on rodent populations and tree seed survival. Oikos 96:402–410

    Article  Google Scholar 

  • Sherry RA, Zhou X, Gu S et al (2007) Divergence of reproductive phenology under climate warming. Proc Natl Acad Sci USA 104:198–202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shibata M, Tanaka H, Nakashizuka T (1998) Causes and consequences of mast seed production of four co-occurring Carpinus species in Japan. Ecology 79:54–64

    Article  Google Scholar 

  • Shibata M, Tanaka H, Iida S et al (2002) Synchronized annual seed production by 16 principal tree species in a temperate deciduous forest, Japan. Ecology 83:1727–1742

    Article  Google Scholar 

  • Silvertown JW (1980) The evolutionary ecology of mast seeding in trees. Biol J Linn Soc 14:235–250

    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

    Article  Google Scholar 

  • Traveset A (1998) Effect of seed passage through vertebrate frugivores’ guts on germination: a review. Perspect Plant Ecol Evol Syst 1:151–190

    Article  Google Scholar 

  • Vander Wall SB, Kuhn KM, Beck MJ (2005) Seed removal, seed predation, and secondary dispersal. Ecology 86:801–806

    Article  Google Scholar 

  • Williams CE (1989) Checklist of North American nut-infesting insects and host plants. J Entomol Sci 24:550–562

    Google Scholar 

  • Yi XF, Yang YQ, Zhang ZB (2010) Intra- and inter-specific effects of mast seeding on seed fates of two sympatric Corylus species. Vegetatio 212:785–793

    Google Scholar 

Download references

Acknowledgments

We would like to thank Norman Christensen, Fred Hain, Matthew Kwit, Megan Mobley, Ram Oren, Carl Salk, Anne Stein, Denis Valle, Kai Zhu, Ines Ibanez, and three anonymous reviewers for comments on the manuscript. The research was supported by NSF Grants BSR-9444146, DEB 9453498, DEB-9632854, DEB-9981392, IDEA-0308498, DEB 0425465, SEII 0430693 and DDDAS 0540347, as well as the USDA Forest Service Pacific Northwest Research Station. The experiments comply with the current laws of the United States of America in which the experiments were performed.

Author contribution statement

DMB and JSC conceived of and designed the study. JSC provided the long-term seed archives and DMB performed measurements. DMB designed and implemented the statistical modeling. DMB and JSC wrote the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David M. Bell.

Additional information

Communicated by Ines Ibanez.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 493 kb)

Supplementary material 2 (TXT 10 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bell, D.M., Clark, J.S. Seed predation and climate impacts on reproductive variation in temperate forests of the southeastern USA. Oecologia 180, 1223–1234 (2016). https://doi.org/10.1007/s00442-015-3537-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-015-3537-6

Keywords

Navigation