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The effect of emerald ash borer-caused tree mortality on the invasive shrub Amur honeysuckle and their combined effects on tree and shrub seedlings

Abstract

Invasive insects and plants are major threats to the health and viability of North American forests. Emerald ash borer (Agrilus planipennis) (EAB) may cause extensive changes to forest composition due to rapid ash (Fraxinus spp.) mortality. Invasive shrubs like Amur honeysuckle (Lonicera maackii) may benefit from EAB and have negative effects on woody seedlings. We predict that ash mortality has positive effects on seedling abundance, recruitment, and survival, but that these effects are influenced by L. maackii basal area and/or cover. We sampled 16 sites, representing a chronosequence of ash mortality throughout western Ohio. We tested whether L. maackii growth and fecundity varied in relation to ash decline. We also investigated effects of ash decline, stand basal area (BA), L. maackii BA and percent cover on woody seedling abundance, recruitment, and survival using linear mixed models evaluated with Akaike’s Information Criterion. These same responses were also investigated for four seedling groups: L. maackii, invasive plants (excluding L. maackii), shade tolerant natives, and shade intolerant natives. We found a significant positive relationship between ash decline and L. maackii BA growth. Lower seedling species richness corresponded with greater L. maackii BA and better ash condition. Greater L. maackii BA was also associated with lower seedling abundance and recruitment, as well as abundance and recruitment of shade-tolerant species, and recruitment of shade-intolerant species. Sites with poorer ash condition and greater L. maackii BA had more L. maackii seedlings. These findings indicate that the negative effects of L. maackii are more important to future forest composition than ash decline; however ash decline increases L. maackii growth, hence exacerbating the effects of this invasive shrub.

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Abbreviations

BA:

Basal area

EAB:

Emerald ash borer

DBH:

Diameter at breast height

ADI:

Ash Decline Index

AMI:

Ash Mortality Index

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Acknowledgements

We thank the land managers of the study sites for permitting access and allowing this work to be conducted within the research plots. We thank the following funding sources: Botanical Society of America Graduate Student Research Award, Sigma Xi, and the Academic Challenge programs of the Miami University Botany and Biology Departments. We thank the many field technicians that assisted in data collection and entry. In particular we would like to thank Erik DeBurgomaster, Matt Higham, Dane Weeks, Gary Hoven, Justin Hoven, Britton Flash, Charles Flower, Robert Ford, Tim Fox, Benjamin Gombash, Rachel Hefflinger, Sagar Jasani, Joan Jolliff, Parker Jones, Scott Kelsey, Tom Macy, Mike Marshall, Elizabeth Monarch, Zak Morvay, Rachel Kappler, Sarah Starr, Samuel Stroebel, Joel Throckmorton, and Bernadette Wiggin. Long-term monitoring plot data collection was supported by the USDA Forest Service and USDA APHIS. We also thank Annemarie Smith, Daniel A. Herms, Robert P. Long, and Kamal J.K. Gandhi for allowing us to use their figure in Appendix 3, and two anonymous reviewers for valuable comments on an earlier draft of this manuscript.

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Correspondence to Brian M. Hoven.

Appendices

Appendix 1

See Table 2.

Table 2 Location and summary data for 48 plots (16 sites) for data collection on EAB-caused ash decline and woody plant growth responses in central and southwestern Ohio, USA (2012–2014)

Appendix 2

See Fig. 5.

Fig. 5
figure5

Three circular 400 m2 plots were nested within each of the 16 sites. Within the plot all canopy trees ≥10 cm diameter at breast height (DBH) were identified and DBH was annually measured, additionally the health of each ash was assessed (Appendix 3). Nested within each site was a 200 m2 sub-plot (circular dashed line) where percent cover of Lonicera maackii was measured annually. Additionally, up to eight L. maackii shrubs (two per quadrant) were tagged, basal diameter and fecundity was measured. Within the four 4 m2 micro-plots located in each cardinal direction 6 m from the center of each plot all tree and shrub seedlings (20–100 cm) were identified, tagged, and their height was measured. All measurements were conducted in 2012, 2013, and 2014

Appendix 3

See Fig. 6.

Fig. 6
figure6

Ash canopy (>10 cm DBH) health condition scale from Smith et al. (2015). Photo credit: Daniel A. Herms, The Ohio State University. Rating Scale Definitions: 1 a healthy full canopy; 2 thinning canopy, all topmost branches exposed to sunlight have leaves; 3 dieback is evident, thinning canopy, some topmost branches exposed to sunlight are dead (leafless); 4 dieback has occurred on more than 50% of the canopy; 5 canopy completely dead, entire canopy portion of the tree is dead (leafless), epicormics sprouts along the bole do not count

Appendix 4

See Table 3.

Table 3 All seedling species encountered in micro-plots in 16 sites located in central and southwestern Ohio, USA (2012–2014)

Appendix 5

See Fig. 7

Fig. 7
figure7

Frequency distribution of shade tolerance scores (Niinemets and Valladares 2006) for native tree and shrub seedlings 20–100 cm tall censused in 16 deciduous forest sites in Ohio invaded by EAB and Lonicera maackii. We classified those ranked 1–2.99 as shade intolerant and those ranked (3–5) as shade tolerant

Appendix 6

See Table 4.

Table 4 Model comparison results for models testing the effect of EAB-caused ash decline and Lonicera maackii BA and cover on the response of L. maackii fecundity, and for models testing these predictor variables in conjunction with stand density on the response of relative L. maackii seedling growth

Appendix 7

See Table 5.

Table 5 Model comparison results for models testing the effect of EAB-caused ash decline, stand BA, and Lonicera maackii BA and cover on woody seedling species richness (2012–2014) and abundance (2012) of all seedlings and four subsets of seedlings

Appendix 8

See Table 6.

Table 6 Model comparison results for models testing the effect of EAB-caused ash decline, stand BA, and Lonicera maackii BA and cover on woody seedling recruitment (2013 and 2014) of all seedlings and four subsets of seedlings

Appendix 9

See Table 7.

Table 7 Model comparison results for models testing the effect of EAB-caused ash decline, stand BA, and Lonicera maackii BA and cover on woody seedling survival (2012–2014) of all seedlings and four subsets of seedlings

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Hoven, B.M., Gorchov, D.L., Knight, K.S. et al. The effect of emerald ash borer-caused tree mortality on the invasive shrub Amur honeysuckle and their combined effects on tree and shrub seedlings. Biol Invasions 19, 2813–2836 (2017). https://doi.org/10.1007/s10530-017-1485-2

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Keywords

  • Tree fall gap
  • Facilitation
  • Fraxinus
  • Agrilus planipennis
  • Lonicera maackii
  • Seedling recruitment
  • Chronosequence
  • Shade tolerance