Nonnative pests often cause cascading ecological impacts, leading to detrimental socioeconomic consequences; however, how plant diversity may influence insect and disease invasions remains unclear. High species diversity in host communities may promote pest invasions by providing more niches (i.e., facilitation), but it can also diminish invasion success because low host dominance may make it more difficult for pests to establish (i.e., dilution). Most studies to date have focused on small-scale, experimental, or individual pest/disease species, while large-scale empirical studies, especially in natural ecosystems, are extremely rare. Using subcontinental-level data, we examined the role of tree diversity on pest invasion across the conterminous United States and found that the tree-pest diversity relationships are hump-shaped. Pest diversity increases with tree diversity at low tree diversity (because of facilitation or amplification) and is reduced at higher tree diversity (as a result of dilution). Thus, tree diversity likely regulates forest pest invasion through both facilitation and dilution that operate simultaneously, but their relative strengths vary with overall diversity. Our findings suggest the role of native species diversity in regulating nonnative pest invasions.

Department of Forestry and Environmental Resources North Carolina State University Research Triangle Park NC 27709

Department of Forestry and Natural Resources Purdue University West Lafayette IN 47907;

Duke Clinical Research Institute Duke University Durham NC 27705

Faculty of Forestry and Wood Sciences Czech University of Life Sciences Prague CZ 165 21 Praha 6 Suchdol Czech Republic

US Department of Agriculture Forest Service Northern Research Station Morgantown WV 26505

US Department of Agriculture Forest Service Southern Research Station Eastern Forest Environmental Threat Assessment Center Research Triangle Park NC 27709;

See more in PubMed

Keesing F, et al. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature. 2010;468:647–652. PubMed PMC

Simberloff D, et al. Impacts of biological invasions: What’s what and the way forward. Trends Ecol Evol. 2013;28:58–66. PubMed

Liebhold AM, et al. Plant diversity drives global patterns of insect invasions. Sci Rep. 2018;8:12095. PubMed PMC

Smith VH, et al. Crop diversification can contribute to disease risk control in sustainable biofuels production. Front Ecol Environ. 2015;13:561–567.

Boyd IL, Freer-Smith PH, Gilligan CA, Godfray HC. The consequence of tree pests and diseases for ecosystem services. Science. 2013;342:1235773. PubMed

Barbosa P, et al. Associational resistance and associational susceptibility: Having right or wrong neighbors. Annu Rev Ecol Evol Syst. 2009;40:1–20.

Pagán I, et al. Effect of biodiversity changes in disease risk: Exploring disease emergence in a plant-virus system. PLoS Pathog. 2012;8:e1002796. PubMed PMC

Luis AD, Kuenzi AJ, Mills JN. Species diversity concurrently dilutes and amplifies transmission in a zoonotic host-pathogen system through competing mechanisms. Proc Natl Acad Sci USA. 2018;115:7979–7984. PubMed PMC

Salkeld DJ, Padgett KA, Jones JH. A meta-analysis suggesting that the relationship between biodiversity and risk of zoonotic pathogen transmission is idiosyncratic. Ecol Lett. 2013;16:679–686. PubMed PMC

Halliday FW, Heckman RW, Wilfahrt PA, Mitchell CE. A multivariate test of disease risk reveals conditions leading to disease amplification. Proc Biol Sci. 2017;284:20171340. PubMed PMC

Keesing F, Ostfeld RS. Ecology. Is biodiversity good for your health? Science. 2015;349:235–236. PubMed

Haas SE, Hooten MB, Rizzo DM, Meentemeyer RK. Forest species diversity reduces disease risk in a generalist plant pathogen invasion. Ecol Lett. 2011;14:1108–1116. PubMed

Jactel H, Brockerhoff EG. Tree diversity reduces herbivory by forest insects. Ecol Lett. 2007;10:835–848. PubMed

Johnson PT, de Roode JC, Fenton A. Why infectious disease research needs community ecology. Science. 2015;349:1259504. PubMed PMC

Hechinger RF, Lafferty KD. Host diversity begets parasite diversity: Bird final hosts and trematodes in snail intermediate hosts. Proc Biol Sci. 2005;272:1059–1066. PubMed PMC

Johnson PT, et al. Habitat heterogeneity drives the host-diversity-begets-parasite-diversity relationship: Evidence from experimental and field studies. Ecol Lett. 2016;19:752–761. PubMed PMC

Kamiya T, O’Dwyer K, Nakagawa S, Poulin R. Host diversity drives parasite diversity: Meta‐analytical insights into patterns and causal mechanisms. Ecography. 2014;37:689–697.

Lin YP, Cook DH, Gullan PJ, Cook LG. Does host‐plant diversity explain species richness in insects? A test using Coccidae (Hemiptera) Ecol Entomol. 2015;40:299–306.

Johnson PT, Preston DL, Hoverman JT, LaFonte BE. Host and parasite diversity jointly control disease risk in complex communities. Proc Natl Acad Sci USA. 2013;110:16916–16921. PubMed PMC

Civitello DJ, et al. Biodiversity inhibits parasites: Broad evidence for the dilution effect. Proc Natl Acad Sci USA. 2015;112:8667–8671. PubMed PMC

Huang ZY, van Langevelde F, Prins HH, de Boer WF. Dilution versus facilitation: Impact of connectivity on disease risk in metapopulations. J Theor Biol. 2015;376:66–73. PubMed

Guo Q, Fei SL, Potter KM, Liebhold AM. 2019 doi: 10.4231/MM0B-JT53. Data from “ Native Tree and Nonnative Pest (Insect and Pathogen) Species Richness Across the Conterminous United States ” (Purdue University Research Repository, West Lafayette, IN). Available at . . Deposited February 4, 2019. DOI

Liebhold AM, Brockerhoff EG, Garrett LJ, Parke JL, Britton KO. Live plant imports: The major pathway for forest insect and pathogen invasions of the US. Front Ecol Environ. 2012;10:135–143.

Liebhold AM, et al. A highly aggregated geographical distribution of forest pest invasions in the USA. Divers Distrib. 2013;19:1208–1216.

Simberloff D. The role of propagule pressure in biological invasions. Annu Rev Ecol Evol Syst. 2009;40:81–102.

Pyšek P, et al. Disentangling the role of environmental and human pressures on biological invasions across Europe. Proc Natl Acad Sci USA. 2010;107:12157–12162. PubMed PMC

Huang ZYX, van Langevelde F, Estrada-Peña A, Suzán G, DE Boer WF. The diversity-disease relationship: Evidence for and criticisms of the dilution effect. Parasitology. 2016;143:1075–1086. PubMed

Liu X, Lyu S, Zhou S, Bradshaw CJA. Warming and fertilization alter the dilution effect of host diversity on disease severity. Ecology. 2016;97:1680–1689. PubMed

Cline LC, et al. Resource availability underlies the plant-fungal diversity relationship in a grassland ecosystem. Ecology. 2018;99:204–216. PubMed

Johnson PT, Preston DL, Hoverman JT, Richgels KL. Biodiversity decreases disease through predictable changes in host community competence. Nature. 2013;494:230–233. PubMed

Johnson PT, Ostfeld RS, Keesing F. Frontiers in research on biodiversity and disease. Ecol Lett. 2015;18:1119–1133. PubMed PMC

Strona G, Lafferty KD. Environmental change makes robust ecological networks fragile. Nat Commun. 2016;7:12462. PubMed PMC

Watts AG, et al. Host functional connectivity and the spread potential of Lyme disease. Landsc Ecol. 2018;11:1925–1938.

Rottstock T, Joshi J, Kummer V, Fischer M. Higher plant diversity promotes higher diversity of fungal pathogens, while it decreases pathogen infection per plant. Ecology. 2014;95:1907–1917. PubMed

Letourneau DK, Jedlicka JA, Bothwell SG, Moreno CR. Effects of natural enemy biodiversity on the suppression of arthropod herbivores in terrestrial ecosystems. Annu Rev Ecol Evol Syst. 2009;40:573–592.

Richards LA, et al. Phytochemical diversity drives plant-insect community diversity. Proc Natl Acad Sci USA. 2015;112:10973–10978. PubMed PMC

Becerra JX. On the factors that promote the diversity of herbivorous insects and plants in tropical forests. Proc Natl Acad Sci USA. 2015;112:6098–6103. PubMed PMC

Bebber DP. Range-expanding pests and pathogens in a warming world. Annu Rev Phytopathol. 2015;53:335–356. PubMed

Mitchell CE, Tilman D, Groth JV. Effects of grassland plant species diversity, abundance, and composition on foliar fungal disease. Ecology. 2002;83:1713–1726.

Hudgins EJ, Liebhold AM, Leung B. Predicting the spread of all invasive forest pests in the United States. Ecol Lett. 2017;20:426–435. PubMed

Merow C, Bois ST, Allen JM, Xie Y, Silander JA., Jr Climate change both facilitates and inhibits invasive plant ranges in New England. Proc Natl Acad Sci USA. 2017;114:E3276–E3284. PubMed PMC

Reams G, et al. 2005. The forest inventory and analysis sampling frame. The enhanced forest inventory and analysis program-national sampling design and estimation procedures, eds Bechtold WA, Patterson PL (US Department of Agriculture, Asheville, NC), General Technical Reports SRS-80, pp 11–26.

Cohen JM, et al. Spatial scale modulates the strength of ecological processes driving disease distributions. Proc Natl Acad Sci USA. 2016;113:E3359–E3364. PubMed PMC

Grace JB. Structural Equation Modeling and Natural Systems. Cambridge Univ Press; Cambridge, UK: 2006.

Cade BS, Guo QF. Estimating effects of constraints on plant performance with regression quantiles. Oikos. 2000;91:245–254.

Global proliferation of nonnative plants is a major driver of insect invasions

Climate affects the outbreaks of a forest defoliator indirectly through its tree hosts