Variable effects of forest diversity on invasions by non-native insects and pathogens

Ward, Samuel F.; Liebhold, Andrew M.; Fei, Songlin

doi:10.1007/s10531-022-02443-4

Original Paper
Published: 25 June 2022

Variable effects of forest diversity on invasions by non-native insects and pathogens

Biodiversity and Conservation (2022)Cite this article

165 Accesses
Metrics details

Abstract

The geographical distributions of non-native forest insects and pathogens (pests) result from a multitude of interacting abiotic and biotic factors. Following arrival, the presence of suitable host trees and environmental conditions are required for pests to establish and spread, but the role of forest biodiversity in this process is not well-understood. We analyzed county-level data for 22 non-native forest pests in the conterminous United States, developing species-specific models to investigate the effects of spatial contagion, human activities, and host and non-host tree biomass or richness on the occurrence of pest species. Species-specific models indicated that (i) the spatial contagion of invasions was the most common driver of invasion incidence, (ii) facilitation effects from host biomass and richness were present in approximately half of the invasions and almost entirely observed in invasions by sap-feeding insects or pathogens, and (iii) there was substantial variation in the direction and magnitude of the effects of non-host tree biomass and richness on invasion. Our analyses highlighted the prominent role of spatially derived propagule pressure in driving intracontinental invasions whereas effects of forest biodiversity were variable and precluded broad generalizations about facilitation and dilution effects as drivers of forest pest invasions at large spatial scales.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Data availability

The data supporting findings of this study are available in the supplementary material (Online Appendix 2).

References

Barbosa P, Hines J, Kaplan I et al (2009) Associational resistance and associational susceptibility: having right or wrong neighbors. Annu Rev Ecol Evol Syst 40:1–20. https://doi.org/10.1146/annurev.ecolsys.110308.120242
Article Google Scholar
Becerra JX (2015) On the factors that promote the diversity of herbivorous insects and plants in tropical forests. Proc Natl Acad Sci 112:6098–6103. https://doi.org/10.1073/pnas.1418643112
CAS Article PubMed PubMed Central Google Scholar
Bechtold W, Patterson P (2005) The enhanced forest inventory and analysis program—national sampling design and estimation procedures. USDA Forest Service General Technical Report
Bosso L, Luchi N, Maresi G et al (2017) Predicting current and future disease outbreaks of Diplodia sapinea shoot blight in Italy: species distribution models as a tool for forest management planning. For Ecol Manag 400:655–664. https://doi.org/10.1016/j.foreco.2017.06.044
Article Google Scholar
Branco M, Nunes P, Roques A et al (2019) Urban trees facilitate the establishment of non-native forest insects. NeoBiota 52:25–46. https://doi.org/10.3897/neobiota.52.36358
Article Google Scholar
Brockerhoff EG, Barbaro L, Castagneyrol B et al (2017) Forest biodiversity, ecosystem functioning and the provision of ecosystem services. Biodivers Conserv 26:3005–3035. https://doi.org/10.1007/s10531-017-1453-2
Article Google Scholar
Castagneyrol B, Giffard B, Péré C, Jactel H (2013) Plant apparency, an overlooked driver of associational resistance to insect herbivory. J Ecol 101:418–429. https://doi.org/10.1111/1365-2745.12055
Article Google Scholar
Castagneyrol B, Kozlov MV, Poeydebat C et al (2020) Associational resistance to a pest insect fades with time. J Pest Sci 93:427–437. https://doi.org/10.1007/s10340-019-01148-y
Article Google Scholar
Colunga-Garcia M, Haack RA, Adelaja AO (2009) Freight transportation and the potential for invasions of exotic insects in urban and periurban forests of the United States. J Econ Entomol 102:237–246. https://doi.org/10.1603/029.102.0133
Article PubMed Google Scholar
Colunga-Garcia M, Haack RA, Magarey RA, Margosian ML (2010) Modeling spatial establishment patterns of exotic forest insects in urban areas in relation to tree cover and propagule pressure. J Econ Entomol 103:108–118. https://doi.org/10.1603/EC09203
Article PubMed Google Scholar
Delibes M, Gaona P, Ferreras P (2001) Effects of an attractive sink leading into maladaptive habitat selection. Am Nat 158:277–285. https://doi.org/10.1086/321319
CAS Article PubMed Google Scholar
Dormann CF, Elith J, Bacher S et al (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46. https://doi.org/10.1111/j.1600-0587.2012.07348.x
Article Google Scholar
Elton CS (1958) Ecology of invasions by animals and plants. Methuen Publishing, Boston
Book Google Scholar
Fargione JE, Tilman D (2005) Diversity decreases invasion via both sampling and complementarity effects. Ecol Lett 8:604–611. https://doi.org/10.1111/j.1461-0248.2005.00753.x
Article Google Scholar
Fridley JD, Stachowicz JJ, Naeem S et al (2007) The invasion paradox: reconciling pattern and process in species invasions. Ecology 88:3–17. https://doi.org/10.1890/0012-9658(2007)88[3:TIPRPA]2.0.CO;2
CAS Article PubMed Google Scholar
Gripenberg S, Mayhew PJ, Parnell M, Roslin T (2010) A meta-analysis of preference-performance relationships in phytophagous insects. Ecol Lett 13:383–393. https://doi.org/10.1111/j.1461-0248.2009.01433.x
Article PubMed Google Scholar
Guo Q, Fei S, Potter KM et al (2019) Tree diversity regulates forest pest invasion. Proc Natl Acad Sci 116:7382–7386. https://doi.org/10.1073/pnas.1821039116
CAS Article PubMed PubMed Central Google Scholar
Guyot V, Castagneyrol B, Vialatte A et al (2016) Tree diversity reduces pest damage in mature forests across Europe. Biol Lett 12:20151037. https://doi.org/10.1098/rsbl.2015.1037
Article PubMed PubMed Central Google Scholar
Haack RA (2020) Where have all the pine shoot beetles gone, long time passing? The 1992 PSB federal quarantine is coming to an end. Newsl Michigan Entomol Soc 64:1–3
Google Scholar
Haas SE, Hooten MB, Rizzo DM, Meentemeyer RK (2011) Forest species diversity reduces disease risk in a generalist plant pathogen invasion. Ecol Lett 14:1108–1116. https://doi.org/10.1111/j.1461-0248.2011.01679.x
Article PubMed Google Scholar
Hudgins EJ, Liebhold AM, Leung B (2017) Predicting the spread of all invasive forest pests in the United States. Ecol Lett 20:426–435. https://doi.org/10.1111/ele.12741
Article PubMed Google Scholar
Iannone BV, Oswalt CM, Liebhold AM et al (2015) Region-specific patterns and drivers of macroscale forest plant invasions. Divers Distrib 21:1181–1192. https://doi.org/10.1111/ddi.12354
Article Google Scholar
Iannone BV, Potter KM, Dixon Hamil K-A et al (2016) Evidence of biotic resistance to invasions in forests of the Eastern USA. Landsc Ecol 31:85–99. https://doi.org/10.1007/s10980-015-0280-7
Article Google Scholar
Jactel H, Brockerhoff EG (2007) Tree diversity reduces herbivory by forest insects. Ecol Lett 10:835–848. https://doi.org/10.1111/j.1461-0248.2007.01073.x
Article PubMed Google Scholar
Jactel H, Menassieu P, Vetillard F et al (2006) Tree species diversity reduces the invasibility of maritime pine stands by the bast scale, Matsucoccus feytaudi (Homoptera: Margarodidae). Can J for Res 36:314–323. https://doi.org/10.1139/x05-251
Article Google Scholar
Jactel H, Moreira X, Castagneyrol B (2021) Tree diversity and forest resistance to insect pests: patterns, mechanisms, and prospects. Annu Rev Entomol 66:277–296. https://doi.org/10.1146/annurev-ento-041720-075234
CAS Article PubMed Google Scholar
Koch FH (2021) Considerations regarding species distribution models for forest insects. Agric for Entomol 23:393–399. https://doi.org/10.1111/afe.12458
Article Google Scholar
Koch FH, Ambrose MJ, Yemshanov D et al (2018) Modeling urban distributions of host trees for invasive forest insects in the eastern and central USA: a three-step approach using field inventory data. For Ecol Manag 417:222–236. https://doi.org/10.1016/j.foreco.2018.03.004
Article Google Scholar
Levine JM, D’Antonio CM (1999) Elton revisited: a review of evidence linking diversity and invasibility. Oikos 87:15–26. https://doi.org/10.2307/3546992
Article Google Scholar
Liebhold AM, Mccullough DG, Blackburn LM et al (2013) A highly aggregated geographical distribution of forest pest invasions in the USA. Divers Distrib 19:1208–1216. https://doi.org/10.1111/ddi.12112
Article Google Scholar
Liebhold AM, Yamanaka T, Roques A et al (2018) Plant diversity drives global patterns of insect invasions. Sci Rep 8:12095. https://doi.org/10.1038/s41598-018-30605-4
CAS Article PubMed PubMed Central Google Scholar
MacArthur R (1955) Fluctuations of animal populations and a measure of community stability. Ecology 36:533–536. https://doi.org/10.2307/1929601
Article Google Scholar
Mally R, Ward SF, Trombik J et al (2021) Non-native plant drives the spatial dynamics of its herbivores: the case of black locust (Robinia pseudoacacia) in Europe. NeoBiota 69:155–175. https://doi.org/10.3897/neobiota.69.71949
Article Google Scholar
May R (1975) Patterns of species abundance and diversity. In: Cody ML, Diamond JM (eds) Ecology and evolution of communities. Harvard Univ. Press, Harvard
Google Scholar
Morin RS, Liebhold AM, Tobin PC et al (2007) Spread of beech bark disease in the eastern United States and its relationship to regional forest composition. Can J for Res 37:726–736. https://doi.org/10.1139/X06-281
Article Google Scholar
Morin RS, Liebhold AM, Gottschalk KW (2009) Anisotropic spread of hemlock woolly adelgid in the eastern United States. Biol Invasions 11:2341–2350. https://doi.org/10.1007/s10530-008-9420-1
Article Google Scholar
Naeem S, Li S (1997) Biodiversity enhances ecosystem reliability. Nature 390:507–509. https://doi.org/10.1038/37348
CAS Article Google Scholar
Naeem S, Knops JMH, Tilman D et al (2000) Plant diversity increases resistance to invasion in the absence of covarying extrinsic factors. Oikos 91:97–108. https://doi.org/10.1034/j.1600-0706.2000.910108.x
Article Google Scholar
Panzavolta T, Bracalini M, Benigno A, Moricca S (2021) Alien invasive pathogens and pests harming trees, forests, and plantations: pathways, global consequences and management. Forests 12:1364. https://doi.org/10.3390/f12101364
Article Google Scholar
Prospero S, Cleary M (2017) Effects of host variability on the spread of invasive forest diseases. Forests 8:80. https://doi.org/10.3390/f8030080
Article Google Scholar
Richards LA, Dyer LA, Forister ML et al (2015) Phytochemical diversity drives plant–insect community diversity. Proc Natl Acad Sci 112:10973–10978. https://doi.org/10.1073/pnas.1504977112
CAS Article PubMed PubMed Central Google Scholar
Rigot T, van Halder I, Jactel H (2014) Landscape diversity slows the spread of an invasive forest pest species. Ecography 37:648–658. https://doi.org/10.1111/j.1600-0587.2013.00447.x
Article Google Scholar
Riley CB, Raupp MJ, Fite KL et al (2022) Woody plant biodiversity explains arthropod pest management interventions in residential landscapes. Urban for Urban Green 67:127439. https://doi.org/10.1016/j.ufug.2021.127439
Article Google Scholar
Rosenthal LM, Simler-Williamson AB, Rizzo DM (2021) Community-level prevalence of a forest pathogen, not individual-level disease risk, declines with tree diversity. Ecol Lett 24:2477–2489. https://doi.org/10.1111/ele.13871
Article PubMed Google Scholar
Rottstock T, Joshi J, Kummer V, Fischer M (2014) Higher plant diversity promotes higher diversity of fungal pathogens, while it decreases pathogen infection per plant. Ecology 95:1907–1917. https://doi.org/10.1890/13-2317.1
Article PubMed Google Scholar
Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Syst 40:81–102. https://doi.org/10.1146/annurev.ecolsys.110308.120304
Article Google Scholar
Srivastava V, Roe AD, Keena MA et al (2021) Oh the places they’ll go: improving species distribution modelling for invasive forest pests in an uncertain world. Biol Invasions 23:297–349. https://doi.org/10.1007/s10530-020-02372-9
Article Google Scholar
Stohlgren TJ, Barnett DT, Kartesz JT (2003) The rich get richer: patterns of plant invasions in the United States. Front Ecol Environ 1:11–14. https://doi.org/10.2307/3867959
Article Google Scholar
Tilman D, Downing JA (1994) Biodiversity and stability in grasslands. Nature 367:363–365. https://doi.org/10.1038/367363a0
Article Google Scholar
US Census Bureau (2010) United States Census Bureau. https://www2.census.gov/programs-surveys/popest/datasets/2010-2017/counties/totals/
Ward SF, Fei S, Liebhold AM (2019) Spatial patterns of discovery points and invasion hotspots of non-native forest pests. Glob Ecol Biogeogr 28:1749–1762. https://doi.org/10.1111/geb.12988
Article Google Scholar
Ward SF, Fei S, Liebhold AM (2020) Temporal dynamics and drivers of landscape-level spread by emerald ash borer. J Appl Ecol 57:1020–1030. https://doi.org/10.1111/1365-2664.13613
Article Google Scholar

Download references

Acknowledgements

We thank survey crews, technicians, and scientists from the USDA FIA program for collecting and managing forest inventory data. We also thank the handling editor and an anonymous reviewer for insightful comments that improved the manuscript.

Funding

This research was supported by National Science Foundation Macrosystems Biology Grant 1638702, the USDA Forest Service, and grant EVA4.0, No. CZ.02.1.01/0.0/0.0/16_019/0000803 financed by Czech Operational Programme "Science, Research, and Education.” This publication is a contribution of the Mississippi Agricultural and Forestry Experiment Station and based upon work supported by the National Institute of Food and Agriculture, U.S. Department of Agriculture, Hatch project under accession number 1025843.

Author information

Authors and Affiliations

Department of Biochemistry, Molecular Biology, Entomology, and Plant Pathology, Mississippi State University, Mississippi State, MS, 39762, USA
Samuel F. Ward
USDA Forest Service, Northern Research Station, Morgantown, WV, 26505, USA
Andrew M. Liebhold
Faculty of Forestry and Wood Sciences, Czech University of Life Sciences Prague, 165 00, Prague 6, Suchdol, Czech Republic
Andrew M. Liebhold
Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN, 47907, USA
Songlin Fei

Authors

Samuel F. Ward
View author publications
You can also search for this author in PubMed Google Scholar
Andrew M. Liebhold
View author publications
You can also search for this author in PubMed Google Scholar
Songlin Fei
View author publications
You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception, data curation, and analyses. The first draft of the manuscript was written by SFW and all authors provided substantial input on subsequent versions. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Samuel F. Ward.

Ethics declarations

Competing interest

The authors have no relevant financial or non-financial interests to disclose.

Additional information

Communicated by B. D. Hoffmann.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article belongs to the Topical Collection: Forest and plantation biodiversity.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 82 kb)

Supplementary file2 (CSV 11033 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Ward, S.F., Liebhold, A.M. & Fei, S. Variable effects of forest diversity on invasions by non-native insects and pathogens. Biodivers Conserv (2022). https://doi.org/10.1007/s10531-022-02443-4

Download citation

Received: 06 December 2021
Revised: 19 May 2022
Accepted: 30 May 2022
Published: 25 June 2022
DOI: https://doi.org/10.1007/s10531-022-02443-4

Keywords

Biodiversity
Forest insect
Habitat invasibility
Invasion
Pathogen
Species richness
Spread