Skip to main content
Log in

Chronic herbivory negatively impacts cone and seed production, seed quality and seedling growth of susceptible pinyon pines

  • Plant Animal Interactions
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Although herbivory often reduces the reproduction of attacked trees, few studies have examined how naturally occurring insect-resistant and susceptible trees differ in their reproduction, nor have these effects been experimentally examined through long-term herbivore removals. In addition, few studies have examined the effects of herbivory on the quality of seeds produced and the implications of reduced seed quality on seedling establishment. We evaluated the impact of chronic herbivory by the stem-boring moth, Dioryctria albovittella, on cone and seed production of the pinyon pine (Pinus edulis) during two mast years. Three patterns emerged. First, moth herbivory was associated with reductions in cone production, viable seed production and seed mass. Specifically, pinyons susceptible to moth attack had 93–95% lower cone production, and surviving cones produced 31–37% fewer viable seeds, resulting in a 96–97% reduction in whole tree viable seed production. In addition, surviving seeds from susceptible trees had 18% lower mass than resistant trees. Second, long-term experimental removal of the herbivore resulted in increased rates of cone and seed production and quality, indicating that moth herbivory was the driver of these reductions. Third, seed size was positively associated with seed germination and seedling biomass and height, suggesting that trees suffering chronic herbivory produce poorer quality offspring. Thus, the resistance traits of pinyons can affect the quality of offspring, which in turn may affect subsequent seedling establishment and population dynamics.

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

Access this article

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

Similar content being viewed by others

References

  • Agrawal AA, Laforsch C, Tollrian R (1999) Transgenerational induction of defenses in animals and plants. Nature 401:60–63

    Article  CAS  Google Scholar 

  • Armstrong DP, Westoby M (1993) Seedlings from large seeds tolerate defoliation better: a test using phylogenetically independent contrasts. Ecology 74:1092–1100

    Article  Google Scholar 

  • Beon MS, Bartsch N (2003) Early seedling growth of pine (Pinus densiflora) and oaks (Quercus serrata, Q. mongolica, Q. varabilis) in response to light intensity and soil moisture. Plant Ecol 167:97–105

    Article  Google Scholar 

  • Bonfil C (1998) The effects of seed size, cotyledon reserves, and herbivory on seedling survival and growth in Quercus rugosa and Q. laurina (Fagaceae). Am J Bot 85:79–87

    Article  Google Scholar 

  • Brown JH, Whitham TG, Morgan-Ernest SK, Gehring CA (2001) Complex species interactions and the dynamics of ecological systems: long-term experiments. Science 293:643–650

    Article  PubMed  CAS  Google Scholar 

  • Castro J (1999) Seed mass versus seedling performance in Scots pine: a maternally dependent trait. New Phytol 144:153–161

    Article  Google Scholar 

  • Christensen KM, Whitham TG (1991) Indirect herbivore mediation of avian seed dispersal in pinyon pine. Ecology 72:534–542

    Article  Google Scholar 

  • Christensen KM, Whitham TG (1993) Impact of insect herbivores on competition between birds and mammals for pinyon pine seeds. Ecology 74:2270–2278

    Article  Google Scholar 

  • Christensen KM, Whitham TG, Balda RP (1991) Discrimination among pinyon pine seeds by Clark’s Nutcrackers: effects of cone crop size and cone characteristics. Oecologia 86:402–407

    Article  Google Scholar 

  • Cobb NS, Mopper S, Gehring, CA, Caouette M, Christensen KM, Whitham TG (1997) Increased moth herbivory associated with environmental stress of pinyon pine at local and regional levels. Oecologia 109:389–397

    Article  Google Scholar 

  • Cobb NS, Trotter III RT, Whitham TG (2002) Long-term sexual allocation in herbivore resistant and susceptible pinyon pine. Oecologia 130:78–87

    Google Scholar 

  • Crawley MJ (1983) Herbivory: the dynamics of animal-plant interactions. Blackwell, Oxford

    Google Scholar 

  • Gehring CA, Whitham TG (1991) Herbivore-driven mycorrhizal mutualism in insect-susceptible pinyon pine. Nature 353:556–557

    Article  Google Scholar 

  • Gehring CA, Whitham TG (1994) Comparisons of ectomycorrhizae on pinyon pine (Pinus edulis; Pinaceae) across extremes of soil type and herbivory. Am J Bot 81:1509–1516

    Article  Google Scholar 

  • Gehring CA, Whitham TG (2002) Mycorrhiza-herbivore interactions: population and community consequences. In: van der Heijden MGA, Sanders IR (eds) Mycorrhizal ecology. Springer, Berlin Heidelderg New York, pp 295–320

    Google Scholar 

  • Gomez JM (2004) Bigger is not always better: conflicting selective pressures on seed size in Quercus ilex. Evolution 58:71–80

    PubMed  Google Scholar 

  • Green JJ, Newberry DM (2001) Light and seed size affect establishment of grove-forming ectomycorrhizal rain forest tree species. New Phytol 151:271–289

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Hutchings MJ (1997) The structure of plant populations. In: Crawley MJ (ed.) Plant ecology, 2nd edn. Blackwell, Oxford, pp 325–358

    Google Scholar 

  • Kaitaniemi P, Neuvonen S, Nyyssönen T (1999) Effects of cumulative defoliations on growth, reproduction, and insect resistance in mountain birch. Ecology 80:524–532

    Google Scholar 

  • Khan ML, Shankar U (2001) Effect of seed weight, light regime and substratum microsite on germination and seedling growth of Quercus semiserrata Roxb. Trop Ecol 42:117–125

    Google Scholar 

  • Leishman M, Westoby M (1994) The role of large seeds in seedling establishment in dry soil conditions: experimental evidence from semi-arid species. J Ecol 82:249–258

    Article  Google Scholar 

  • Leishmen M (2001) Does the seed size/number trade-off model determine plant community structure? An assessment of the model mechanisms and their generality. Oikos 94:294–302

    Article  Google Scholar 

  • Logan JA, Régnière J, Powell JA (2003) Assessing the impacts of global warming on forest pest dynamics. Front Ecol Environ 1:130–137

    Google Scholar 

  • Louda SM, Potvin MA (1995) Effect of inflorescence-feeding insects on the demography and lifetime fitness of a native plant. Ecology 76:229–245

    Article  Google Scholar 

  • Maron JL (1998) Insect herbivory above- and belowground: individual and joint effects on plant fitness. Ecology 79:1281–1293

    Google Scholar 

  • McLemore BF (1965) Pentane flotation for separating full and empty longleaf pine seeds. For Sci 14:219–221

    Google Scholar 

  • Mopper S, Mitton J, Whitham TG, Cobb NS, Christensen KM (1991) Genetic differentiation and heterozygosity in pinyon pine associated with herbivory and environmental stress. Evolution 45:989–999

    Article  Google Scholar 

  • Muthumukar T, Udaiyan K (2000) The role of seed reserves in arbuscular mycorrhizal formation and growth of Leucaena leucocephala (Lam.) de Wit and Zea mays L. Mycorrhiza 9:323–330

    Article  Google Scholar 

  • Obeso JR (1993) Does defoliation affect reproductive output of herbaceous perrenials and woody plants in different ways?. Funct Ecol 7:150–155

    Article  Google Scholar 

  • Obeso JR (2002) The costs of defense in plants. New Phytol 155:321–349

    Article  Google Scholar 

  • Ruel J, Whitham TG (2002) Fast-growing juvenile pinyons suffer greater herbivory when mature. Ecology 83:2691–2699

    Article  Google Scholar 

  • Salleo S, Nardini A, Raimondo F, Lo Gullo MA, Pace F, Giacomich P (2003) Effects of defoliation cause by the lead miner Cameraria ohridella on wood production and efficiency in Aesculus hippocastanum growing in north-eastern Italy. Trees 17:367–375

    Google Scholar 

  • Strauss SY (1991) Direct, indirect, and cumulative effects of three native herbivores on a shared host plant. Ecology 72:543–558

    Article  Google Scholar 

  • Thalmann C, Freise J, Heitland W, Bacher S (2003) Effects of defoliation by horse chestnut leafminer (Camararia ohridella) on reproduction in Aesculus hippocastanum. Tree Struct Funct 17:383–388

    Article  Google Scholar 

  • Turnbull LA, Crawley MJ, Rees M (2000) Are plant populations seed-limited? A review of seed sowing experiments. Oikos 88:225–238

    Article  Google Scholar 

  • Vander Wall SB (1997) Dispersal of singleleaf pinon pine (Pinus monophylla) by seed caching rodents. J Mamm 78:181–191

    Article  Google Scholar 

  • Vander Wall SB (2003) Effect of seed size of wind-dispersed pines (Pinus) on secondary seed dispersal and the caching behavior of rodents. Oikos 100:23–34

    Article  Google Scholar 

  • Weiner J (1990) Asymmetric competition in plant populations. Trends Ecol Evol 5:360–364

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Whitham TG, Young WP, Martinsen GD, Gehring CA, Schweitzer JA, Shuster SM, Wimp GM, Fischer DG, Bailey JK, Lindroth RL, Woolbright S, Kuske CR (2003) Community and ecosystem genetics: a consequence of the extended phenotype. Ecology 84:559–573

    Article  Google Scholar 

Download references

Acknowledgements

We thank N. Cobb, K. Christensen, S. Mopper and the Gehring and Whitham lab groups for field and laboratory assistance. This research was funded by USDA grant 92-37302-7854, and NSF grants DEB-0236204, and DEB-0415563. All experiments comply with current laws of the USA.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rebecca C. Mueller.

Additional information

Communicated by Louis Pitelka

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mueller, R.C., Wade, B.D., Gehring, C.A. et al. Chronic herbivory negatively impacts cone and seed production, seed quality and seedling growth of susceptible pinyon pines. Oecologia 143, 558–565 (2005). https://doi.org/10.1007/s00442-005-0029-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-005-0029-0

Keywords

Navigation