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The relative influences of host plant genotype and yearly abiotic variability in determining herbivore abundance

  • Plant-Animal interactions - Original Paper
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Abstract

Both plant genotype and yearly abiotic variation affect herbivore population sizes, but long-term data have rarely been used to contrast the relative contributions of each. Using a hierarchical Bayesian model, we directly compare effects of these two factors on the population size of a common herbivore, Aceria parapopuli, on Populus angustifolia × fremontii F1 hybrid trees growing in a common garden across 8 years. Several patterns emerged. First, the Bayesian posterior estimates of tree genotype effects on mite gall number ranged from 0.0043 to 229 on a linear scale. Second, year effect sizes across 8 years of study ranged from 0.133 to 1.895. Third, in comparing the magnitudes of genotypic versus yearly variation, we found that genotypic variation was over 130 times greater than variation among years. Fourth, precipitation in the previous year negatively affected gall abundances, but was minimal compared to tree genotype effects. These findings demonstrate the relative importance of tree genotypic variation in determining herbivore population size. However, given the demonstrated sensitivity of cottonwoods to drought, the loss of individual tree genotypes from an altered climate would have catastrophic impacts on mites that are dependent upon these genotypes for their survival.

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References

  • Amrine JW, Stasny TA (1994) Catalog of the Eriophyoidea (Acarina; Prostigmata) of the World. Indira, West Bloomfield

    Google Scholar 

  • Andrewartha HG, Birch LC (1954) The distribution and abundance of animals. University of Chicago Press, Chicago

    Google Scholar 

  • Baker EO, Kono T, Amrine JW, Delfinado-Baker M, Stasny TA (1996) Eriophyoid mites of the United States. Indira, West Bloomfield

    Google Scholar 

  • Bale JS, Masters GJ, Hodkinson ID, et al. (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob Change Biol 8:1–16. doi:10.1046/j.1365-2486.2002.00451.x

    Article  Google Scholar 

  • Bergh JC (2001) Ecology and aerobiology of dispersing citrus rust mites (Acari: Eriophyidae) in central Florida. Environ Entomol 30:318–326

    Article  Google Scholar 

  • Chandrapatya A, Baker GT (1986) Biological aspects of the geranium mites, Coptophylla caroliniani and Aceria mississippiensis (Prostigmata: Eriophyidae). Exp App Acarol 2:201–216. doi:10.1007/BF01193952

    Article  Google Scholar 

  • Clark JS (2007) Statistical computation for environmental sciences in R: lab manual for models for ecological data. Princeton University Press, Princeton

    Google Scholar 

  • Clark J, LaDeau S (2004) Synthesizing ecological experiments and observational data with hierarchical Bayes. In: Clark J, Gelfand A (eds) Hierarchical modelling for the environmental sciences: statistical methods and applications. Oxford University Press, Oxford, pp 41–58

    Google Scholar 

  • Coley PD (1983) Intraspecific variation in herbivory on two tropical tree species. Ecology 64:426–433. doi:10.2307/1939960

    Article  Google Scholar 

  • Crawford KM, Crutsinger GM, Sanders NJ (2007) Host plant genotypic diversity mediates the distribution of an ecosystem engineer. Ecology 88:2114–2120. doi:10.1890/06-1441.1

    Article  PubMed  Google Scholar 

  • Drouin JA, Langor DW (1992) Poplar bud gall mite. Forestry Leaflet 15, Forestry Canada, Northwestern Region, Northern Forest Centre. Edmonton, Alberta

    Google Scholar 

  • Egan SP, Ott JR (2007) Host plant quality and local adaptation determine the distribution of a gall-forming herbivore. Ecology 88:2868–2879. doi:10.1890/06-1303.1

    Article  PubMed  Google Scholar 

  • English-Loeb GM (1990) Plant drought stress and outbreaks of spider mites: a field test. Ecology 71:1401–1411. doi:10.2307/1938277

    Article  Google Scholar 

  • Evans LM, Allan GJ, Shuster SM et al (2008) Tree hybridization and genotypic variation 658 drive cryptic speciation of a specialist mite herbivore. Evolution 62:3027–3040

    Google Scholar 

  • Floate KD, Kearsley MJC, Whitham TG (1993) Elevated herbivory in plant hybrid zones: Chrysomela confluens, Populus and phenological sinks. Ecology 74:2056–2065. doi:10.2307/1940851

    Article  Google Scholar 

  • Gelman A, Hill J (2007) Data analysis using regression and multilevel/hierarchical models. Cambridge University Press, Cambridge

    Google Scholar 

  • Helms SE, Hunter MD (2005) Variation in plant quality and the population dynamics of herbivore: there is nothing average about aphids. Oecologia 145:197–204. doi:10.1007/s00442-005-0060-1

    Article  PubMed  Google Scholar 

  • Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–732

    Google Scholar 

  • Kalischuk AR, Gom LA, Floate KD, Rood SB (1997) Intersectional cottonwood hybrids are particularly susceptible to the poplar bud gall mite. Can J Bot 75:1349–1355. doi:10.1139/b97-847

    Article  Google Scholar 

  • Karban R (1989) Fine-scale adaptation of herbivorous thrips to individual host plants. Nature 340:60–61. doi:10.1038/340060a0

    Article  Google Scholar 

  • Keith AR, Bailey JK, Whitham TG (2010) A genetic basis to community repeatability and stability. Ecology 11:3398–3406

    Article  Google Scholar 

  • Kiefer HH (1940) Eriophyid studies VIII. Bull Calif Dep Agr 29:21–46

    Google Scholar 

  • Kingsolver JG (1989) Weather and the population dynamics of insects: integrating physiological and population ecology. Physiol Zool 62:314–334

    Google Scholar 

  • Larson KC, Whitham TG (1991) Manipulation of food resources by a gall-forming aphid: the physiology of sink-source interactions. Oecologia 88:15–21. doi:10.1007/BF00328398

    Article  Google Scholar 

  • Larson KC, Whitham TG (1997) Competition between gall aphids and natural plant sinks: plant architecture affects resistance to galling. Oecologia 109:575–582. doi:10.1007/s004420050119

    Article  Google Scholar 

  • Lombardero MJ, Ayres MP, Hofstetter RW, Moser JC, Klepzig KD (2003) Strong indirect interactions of Tarsonemus mites (Acarina, Tarsonemidae) and Dendroctonus frontalis (Coleoptera: Scolytidae). Oikos 102:243–252

    Google Scholar 

  • Louda SM, Collinge SK (1992) Plant resistance to insect herbivores: a field test of the environmental stress hypothesis. Ecology 73:153–169. doi:10.2307/1938728

    Article  Google Scholar 

  • Maddox GD, Cappuccino N (1986) Genetic determination of plant susceptibility to an herbivorous insect depends on environmental context. Evolution 40:863–866

    Article  Google Scholar 

  • McIntyre PJ, Whitham TG (2003) Plant genotype affects long-term herbivore population dynamics and extinction: conservation implications. Ecology 84:311–322. doi:10.1890/0012-9658(2003)084

    Article  Google Scholar 

  • Mopper S (1996) Adaptive genetic structure in phytophagous insect populations. Trends Ecol Evol 11:235–238. doi:10.1016/0169-5347(96)10036-7

    Article  PubMed  CAS  Google Scholar 

  • Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos 62:244–251

    Article  Google Scholar 

  • Price PW (2003) Macroevolutionary theory on macroecological patterns. Cambridge University Press, Cambridge

    Google Scholar 

  • Price PW, Hunter MD (2005) Long-term population dynamics of a sawfly show strong bottom-up effects. J Anim Ecol 74:917–925. doi:10.1111/j.1365-2656.2005.00989.x

    Article  Google Scholar 

  • R Development Core Team (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. URL http://www.R-project.org

  • Régnière J, Bentz B (2007) Modeling cold tolerance in the mountain pine beetle, Dendroctonus ponderosae. J Insect Physiol 53:559–572

    Article  PubMed  Google Scholar 

  • Rehill BJ, Whitham TG, Martinsen GD, Schweitzer JA, Bailey JK, Lindroth RL (2006) Developmental trajectories in cottonwood phytochemistry. J Chem Ecol 32:2269–2285

    Article  PubMed  CAS  Google Scholar 

  • Ritchie ME (2000) Nitrogen limitation and trophic versus abiotic influences on insect herbivores in a temperate grassland. Ecology 81:1601–1612

    Google Scholar 

  • Sabelis MW, Brouin J (1996) Evolutionary ecology: life history patterns, food plant choice and dispersal. In: Lindquist EE, Sabelis MW, Bruin J (eds) Eriophyoid mites: their biology, natural enemies, and control. Elsevier, Amsterdam, pp 329–366

    Chapter  Google Scholar 

  • Spiegelhalter DJ, Best NG, Carlin BP, van der Linde A (2002) Bayesian measures of model complexity and fit. J R Stat Soc B 64:583–639

    Article  Google Scholar 

  • Stone GN, Schönrogge K (2003) The adaptive significance of insect gall morphology. Trends Ecol Evol 18:512–521

    Article  Google Scholar 

  • Trotter TR III, Cobb NS, Whitham TG (2008) Arthropod community diversity and trophic structure: a comparison between extremes of plant stress. Ecol Entomol 33:1–11

    Google Scholar 

  • Underwood N, Rausher MD (2000) The effects of host-plant genotype on herbivore population dynamics. Ecology 81:1565–1576. doi:10.1890/0012-9658(2000)081

    Article  Google Scholar 

  • van Mantgem PJ, Stephenson NL, Byrne JC, Daniels LD, Franklin JF, Fulé PZ, Harmon ME, Larson AJ, Smith JM, Taylor AH, Veblen TT (2009) Widespread increase of tree mortality rates in the western United States. Science 323:521–524

    Article  PubMed  Google Scholar 

  • Whitham TG, Martinsen GD, Floate KD, Dungey HS, Potts BM, Keim P (1999) Plant hybrid zones affect biodiversity: tools for a genetic-based understanding of community structure. Ecology 80:416–428. doi:10.1890/0012-9658(1999)080

    Article  Google Scholar 

  • Whitham TG, Young WP, Martinsen GD et al. (2003) Community and ecosystem 843 genetics: a consequence of the extended phenotype. Ecology 84:559–573

    Google Scholar 

  • Whitham TG, Bailey JK, Schweitzer JA et al. (2006) A framework for community and 838 ecosystem genetics: from genes to ecosystems. Nat Rev Genet 7:510–839

    Google Scholar 

  • Whitham TG, Bailey JK, Schweitzer JS, Shuster SM, Bangert RK, LeRoy CJ, Lonsdorf EV, Allan GJ, DiFazio SP, Potts BM, Fischer DG, Gehring CA, Lindroth RL, Marks JC, Hart SC, Wimp GM, Wooley SC (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Genet 7:510–523

    Article  PubMed  CAS  Google Scholar 

  • Whitham TG, Gehring CA, Evans LM, LeRoy CJ, Bangert RK, Schweitzer JA, Allan GJ, Barbour RC, Fischer DG, Potts BM, Bailey JK (2010) A community and ecosystem genetics approach to conservation biology and management. In: DeWoody JA, Bickham JW, Michler C, Nichols K, Rhodes OE, Woeste K (eds) Molecular approaches in natural resource conservation. Cambridge University Press, Cambridge, pp 50–70

    Google Scholar 

  • Yarnes C, Boecklen WJ (2005) Abiotic factors promote plant heterogeneity and influence herbivore performance and mortality in Gambel's Oak (Quercus gambelii, Nutt.). Entomol Exp Appl 114:87–95

    Google Scholar 

  • Ylioja T, Roininen H, Ayres MP, Rousi M, Price PW (1999) Host-driven population dynamics in an herbivorous insect. Proc Nat Acad Sci USA 96:10735–10740

    Article  PubMed  CAS  Google Scholar 

  • Zhao S, Amrine JW (1997) A new method for studying aerial dispersal behavior of eriophyoid mites (Acari: Eriophyoidea). Syst Appl Acarol 2:107–111

    Google Scholar 

Download references

Acknowledgments

We thank the Ogden Nature Center for supporting our common garden experiments. We thank Nathan Lojewski for assistance in the field, and Pat McIntyre and Brett Dickson for helpful discussion. This work was the outcome of the NAU IGERT Statistics and Modeling Course, and we thank the students in the course for helpful discussion. This work was supported by the NSF Integrative Graduate Education and Research Traineeship program, FIBR DEB-0425908, Science Foundation Arizona (SFAz), and Northern Arizona University.

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Correspondence to Luke M. Evans.

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Communicated by Thomas Hoffmeister.

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Evans, L.M., Clark, J.S., Whipple, A.V. et al. The relative influences of host plant genotype and yearly abiotic variability in determining herbivore abundance. Oecologia 168, 483–489 (2012). https://doi.org/10.1007/s00442-011-2108-8

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