Exotic tree species have consistently lower herbivore load in a cross-Atlantic tree biodiversity experiment.

IDENT arthropods associational effects enemy release exotic herbivores herbivory insects native tree diversity

Journal

Ecology
ISSN: 1939-9170
Titre abrégé: Ecology
Pays: United States
ID NLM: 0043541

Informations de publication

Date de publication:
07 2023
Historique:
revised: 02 03 2023
received: 07 09 2022
accepted: 14 03 2023
medline: 4 7 2023
pubmed: 2 5 2023
entrez: 2 5 2023
Statut: ppublish

Résumé

It is commonly expected that exotic plants experience reduced herbivory, but experimental evidence for such enemy release is still controversial. One reason for conflicting results might be that community context has rarely been accounted for, although the surrounding plant diversity may moderate enemy release. Here, we tested the effects of focal tree origin and surrounding tree diversity on herbivore abundance and leaf damage in a cross-Atlantic tree-diversity experiment in Canada and Germany. We evaluated six European tree species paired with six North American congeners in both their native and exotic range, expecting lower herbivory for the exotic tree species in each pair at each site. Such reciprocal experiments have long been called for, but have not been realized thus far. In addition to a thorough evaluation of overall enemy release effects, we tested whether enemy release effects changed with the surrounding tree diversity. Herbivore abundance was indeed consistently lower on exotics across all six tree genera (12 comparisons). This effect of exotic status was independent of the continent, phylogenetic relatedness, and surrounding tree diversity. In contrast, leaf damage associated with generalist leaf chewers was consistently higher on North American tree species. Interestingly, several species of European weevils were the most abundant leaf chewers on both continents and the dominant herbivores at the Canadian site. Thus, most observed leaf damage is likely to reflect the effect of generalist herbivores that feed heavily on plant species with which they have not evolved. At the German site, sap suckers were the dominant herbivores and showed a pattern consistent with enemy release. Taken together, the consistently lower herbivory on exotics on both continents is not purely a pattern of enemy release in the strictest sense, but to some degree additionally reflects the susceptibility of native plants to invasive herbivores. In conclusion, our cross-Atlantic study is consistent with the idea that nonnative trees have generally reduced herbivory, regardless of tree community diversity and species identity, but for different reasons depending on the dominant herbivore guild.

Identifiants

pubmed: 37127925
doi: 10.1002/ecy.4070
doi:

Banques de données

Dryad
['10.5061/dryad.1zcrjdfxd']

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

e4070

Informations de copyright

© 2023 The Authors. Ecology published by Wiley Periodicals LLC on behalf of The Ecological Society of America.

Références

Adams, J. M., W. Fang, R. M. Callaway, D. Cipollini, E. Newell, and Transatlantic Acer Platanoides Invasion Network (TRAIN). 2009. “A Cross-Continental Test of the Enemy Release Hypothesis: Leaf Herbivory on Acer Platanoides (L.) Is Three Times lower in North America than in its Native Europe.” Biological Invasions 11: 1005-16.
Agrawal, A. A., P. M. Kotanen, C. E. Mitchell, A. G. Power, W. Godsoe, and J. Klironomos. 2005. “Enemy Release? An Experiment with Congeneric Plant Pairs and Diverse above- and Belowground Enemies.” Ecology 86: 2979-89.
Ali, J., and A. Agrawal. 2012. “Specialist Versus Generalist Insect Herbivores and Plant Defense.” Trends in Plant Science 17: 293-302.
Ashton, I. W., and M. T. Lerdau. 2008. “Tolerance to Herbivory, and Not Resistance, May Explain Differential Success of Invasive, Naturalized, and Native North American Temperate Vines.” Diversity and Distributions 14: 169-78.
Barbosa, P., J. Hines, I. Kaplan, H. Martinson, A. Szczepaniec, and Z. Szendrei. 2009. “Associational Resistance and Associational Susceptibility: Having Right or Wrong Neighbors.” Annual Review of Ecology, Evolution, and Systematics 40: 1-20.
Bates, D., M. Mächler, B. Bolker, and S. Walker. 2015. “Fitting Linear Mixed-Effects Models Using lme4.” Journal of Statistical Software 67: 1-48.
Belluau, M., A. Paquette, D. Gravel, P. B. Reich, A. Stefanski, and C. Messier. 2021. “Exotics Are more Complementary over Time in Tree Biodiversity-Ecosystem Functioning Experiments.” Functional Ecology 35: 2550-61.
Bertheau, C., E. G. Brockerhoff, G. Roux-Morabito, F. Lieutier, and H. Jactel. 2010. “Novel Insect-Tree Associations Resulting from Accidental and Intentional Biological ‘Invasions’: A Meta-Analysis of Effects on Insect Fitness.” Ecology Letters 13: 506-15.
Berthelot, S., J. Bauhus, C. Dormann, D. Gravel, C. Messier, C. Nock, A. Paquette, P. Reich, and J. Fründ. 2023. “Exotic Tree Species Have Consistently Lower Herbivore Load in a Cross-Atlantic Tree Biodiversity Experiment.” Dryad, Dataset. https://doi.org/10.5061/dryad.1zcrjdfxd.
Berthelot, S., T. Frühbrodt, P. Hajek, C. A. Nock, C. F. Dormann, J. Bauhus, and J. Fründ. 2021. “Tree Diversity Reduces the Risk of Bark Beetle Infestation for Preferred Conifer Species, but Increases the Risk for Less Preferred Hosts.” Journal of Ecology 109: 2649-61.
Bezemer, T. M., J. A. Harvey, and J. T. Cronin. 2014. “Response of Native Insect Communities to Invasive Plants.” Annual Review of Entomology 59: 119-41.
Brändle, M., I. Kühn, S. Klotz, C. Belle, and R. Brandl. 2008. “Species Richness of Herbivores on Exotic Host Plants Increases with Time since Introduction of the Host.” Diversity and Distributions 14: 905-12.
Brooks, M. E., K. Kristensen, K. J. van Benthem, A. Magnusson, C. W. Berg, A. Nielsen, H. J. Skaug, M. Maechler, and B. M. Bolker. 2017. “glmmTMB Balances Speed and Flexibility among Packages for Zero-Inflated Generalized Linear Mixed Modeling.” The R Journal 9: 378-400.
Christophe, A. 2020. “Effet De l'identité et de la Diversité Des Arbres Sur la Diversité Des Ectomycorhizes.” Master thesis, Université du Québec à Montréal, Canada.
Chun, Y. J., M. Van Kleunen, and W. Dawson. 2010. “The Role of Enemy Release, Tolerance and Resistance in Plant Invasions: Linking Damage to Performance.” Ecology Letters 13: 937-46.
Cincotta, C. L., J. M. Adams, and C. Holzapfel. 2009. “Testing the Enemy Release Hypothesis: A Comparison of Foliar Insect Herbivory of the Exotic Norway Maple (Acer Platanoides L.) and the Native Sugar Maple (A. Saccharum L.).” Biological Invasions 11: 379-88.
Colautti, R. I., A. Ricciardi, I. A. Grigorovich, and H. J. MacIsaac. 2004. “Is Invasion Success Explained by the Enemy Release Hypothesis?” Ecology Letters 7: 721-33.
Enders, M., F. Havemann, F. Ruland, M. Bernard-Verdier, J. A. Catford, L. Gómez-Aparicio, S. Haider, et al. 2020. “A Conceptual Map of Invasion Biology: Integrating Hypotheses into a Consensus Network.” Global Ecology and Biogeography 29: 978-91.
Forister, M. L., V. Novotny, A. K. Panorska, L. Baje, Y. Basset, P. T. Butterill, L. Cizek, et al. 2015. “The Global Distribution of Diet Breadth in Insect Herbivores.” Proceedings of the National Academy of Sciences 112: 442-7.
Goßner, M. M., A. Chao, R. I. Bailey, and A. Prinzing. 2009. “Native Fauna on Exotic Trees: Phylogenetic Conservatism and Geographic Contingency in Two Lineages of Phytophages on Two Lineages of Trees.” The American Naturalist 173: 599-614.
Grossman, J. J., J. Cavender-Bares, P. B. Reich, R. A. Montgomery, and S. E. Hobbie. 2019. “Neighborhood Diversity Simultaneously Increased and Decreased Susceptibility to Contrasting Herbivores in an Early Stage Forest Diversity Experiment.” Journal of Ecology 107: 1492-505.
Hartig, F. 2021. “DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models.” https://CRAN.R-project.org/package=DHARMa.
Heger, T., and J. M. Jeschke. 2014. “The Enemy Release Hypothesis as a Hierarchy of Hypotheses.” Oikos 123: 741-50.
Hill, S. B., and P. M. Kotanen. 2009. “Evidence that Phylogenetically Novel Non-indigenous Plants Experience Less Herbivory.” Oecologia 161: 581-90.
Hobbs, R. J., S. Arico, J. Aronson, J. S. Baron, P. Bridgewater, V. A. Cramer, P. R. Epstein, et al. 2006. “Novel Ecosystems: Theoretical and Management Aspects of the New Ecological World Order.” Global Ecology and Biogeography 15: 1-7.
Jactel, H., and E. G. Brockerhoff. 2007. “Tree Diversity Reduces Herbivory by Forest Insects.” Ecology Letters 10: 835-48.
Jactel, H., X. Moreira, and B. Castagneyrol. 2021. “Tree Diversity and Forest Resistance to Insect Pests: Patterns, Mechanisms, and Prospects.” Annual Review of Entomology 66: 277-96.
Johnson, M. T. J., J. A. Bertrand, and M. M. Turcotte. 2016. “Precision and Accuracy in Quantifying Herbivory.” Ecological Entomology 41: 112-21.
Joshi, J., and K. Vrieling. 2005. “The Enemy Release and EICA Hypothesis Revisited: Incorporating the Fundamental Difference between Specialist and Generalist Herbivores.” Ecology Letters 8: 704-14.
Keane, R. M., and M. J. Crawley. 2002. “Exotic Plant Invasions and the Enemy Release Hypothesis.” Trends in Ecology & Evolution 17: 164-70.
Koricheva, J., H. Vehviläinen, J. Riihimäki, K. Ruohomäki, P. Kaitaniemi, and H. Ranta. 2006. “Diversification of Tree Stands as a Means to Manage Pests and Diseases in Boreal Forests: Myth or Reality?” Canadian Journal of Forest Research 36: 324-36.
Kuznetsova, A., P. B. Brockhoff, and R. H. B. Christensen. 2017. “lmerTest Package: Tests in Linear Mixed Effects Models.” Journal of Statistical Software 82: 1-26.
Liu, H., and P. Stiling. 2006. “Testing the Enemy Release Hypothesis: A Review and Meta-Analysis.” Biological Invasions 8: 1535-45.
Lüdecke, D. 2018. “Ggeffects: Tidy Data Frames of Marginal Effects from Regression Models.” Journal of Open Source Software 3: 772.
Meijer, K., M. Schilthuizen, L. Beukeboom, and C. Smit. 2016. “A Review and Meta-Analysis of the Enemy Release Hypothesis in Plant-Herbivorous Insect Systems.” PeerJ 4: e2778.
Meijer, K., H. Zemel, S. Chiba, C. Smit, L. W. Beukeboom, and M. Schilthuizen. 2015. “Phytophagous Insects on Native and Non-native Host Plants: Combining the Community Approach and the Biogeographical Approach.” PLoS One 10: e0125607.
Morrison, W. E., and M. E. Hay. 2011. “Herbivore Preference for Native vs. Exotic Plants: Generalist Herbivores from Multiple Continents Prefer Exotic Plants that are Evolutionarily Naïve.” PLoS One 6: e17227.
Norghauer, J. M., A. R. Martin, E. E. Mycroft, A. James, and S. C. Thomas. 2011. “Island Invasion by a Threatened Tree Species: Evidence for Natural Enemy Release of Mahogany (Swietenia Macrophylla) on Dominica, Lesser Antilles.” PLoS ONE 6: e18790.
Novotny, V., S. E. Miller, L. Baje, S. Balagawi, Y. Basset, L. Cizek, K. J. Craft, et al. 2010. “Guild-Specific Patterns of Species Richness and Host Specialization in Plant-Herbivore Food Webs from a Tropical Forest: Plant-Herbivore Food Webs in Tropical Forest.” Journal of Animal Ecology 79: 1193-203.
Paradis, E., and K. Schliep. 2019. “Ape 5.0: An Environment for Modern Phylogenetics and Evolutionary Analyses in R.” Bioinformatics 35: 525-8.
Parker, J. D., D. E. Burkepile, and M. E. Hay. 2006. “Opposing Effects of Native and Exotic Herbivores on Plant Invasions.” Science 311: 1459-61.
Parker, J. D., D. E. Burkepile, M. J. Lajeunesse, and E. M. Lind. 2012. “Phylogenetic Isolation Increases Plant Success despite Increasing Susceptibility to Generalist Herbivores.” Diversity and Distributions 18: 1-9.
Pearse, I. S., and A. L. Hipp. 2014. “Native Plant Diversity Increases Herbivory to Non-natives.” Proceedings of the Royal Society of London B: Biological Sciences 281: 20141841.
Pinski, R. A., W. J. Mattson, and K. F. Raffa. 2005a. “Host Breadth and Ovipositional Behavior of Adult Polydrusus sericeus and Phyllobius oblongus (Coleoptera: Curculionidae), Nonindigenous Inhabitants of Northern Hardwood Forests.” Environmental Entomology 34: 148-57.
Pinski, R. A., W. J. Mattson, and K. F. Raffa. 2005b. “Composition and Seasonal Phenology of a Nonindigenous Root-Feeding Weevil (Coleoptera: Curculionidae) Complex in Northern Hardwood Forests in the Great Lakes Region.” Environmental Entomology 34: 298-307.
R Core Team. 2020. R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.
Root, R. B. 1973. “Organization of a Plant-Arthropod Association in Simple and Diverse Habitats: The Fauna of Collards (Brassica Oleracea).” Ecological Monographs 43: 95-124.
Schuldt, A., H. Bruelheide, W. Härdtle, T. Assmann, Y. Li, K. Ma, G. von Oheimb, and J. Zhang. 2015. “Early Positive Effects of Tree Species Richness on Herbivory in a Large-Scale Forest Biodiversity Experiment Influence Tree Growth.” Journal of Ecology 103: 563-71.
Schuldt, A., and M. Scherer-Lorenzen. 2014. “Non-native Tree Species (Pseudotsuga menziesii) Strongly Decreases Predator Biomass and Abundance in Mixed-Species Plantations of a Tree Diversity Experiment.” Forest Ecology and Management 327: 10-7.
Strong, D. R., J. H. Lawton, and S. R. Southwood. 1984. “Insects on Plants.” In Community Patterns and Mechanisms. Oxford: Blackwell Scientific Publicatons.
Tallamy, D. W. 2004. “Do Alien Plants Reduce Insect Biomass?” Conservation Biology 18: 1689-92.
Tobner, C. M., A. Paquette, P. B. Reich, D. Gravel, and C. Messier. 2014. “Advancing Biodiversity-Ecosystem Functioning Science Using High-Density Tree-Based Experiments over Functional Diversity Gradients.” Oecologia 174: 609-21.
Underwood, N., B. D. Inouye, and P. A. Hambäck. 2014. “A Conceptual Framework for Associational Effects: When Do Neighbors Matter and how Would we Know?” The Quarterly Review of Biology 89: 1-19.
van Kleunen, M., W. Dawson, F. Essl, J. Pergl, M. Winter, E. Weber, H. Kreft, et al. 2015. “Global Exchange and Accumulation of Non-native Plants.” Nature 525: 100-3.
Vollmann, M. 1954. “Der Schmalbauchrüßler Phyllobius oblongus L. (Col. Curc.) Ein Beitrag zur Biologie und Bekämpfung.” Zeitschrift für Angewandte Entomologie 36: 117-55.
Vor, T., H. Spellmann, A. Bolte, and C. Ammer. 2015. Potenziale und Risiken eingeführter Baumarten. Göttingen: Universitätsverlag Göttingen.
Wein, A., J. Bauhus, S. Bilodeau-Gauthier, M. Scherer-Lorenzen, C. Nock, and M. Staab. 2016. “Tree Species Richness Promotes Invertebrate Herbivory on Congeneric Native and Exotic Tree Saplings in a Young Diversity Experiment.” PLoS One 11: e0168751.
Zvereva, E. L., V. Zverev, and M. V. Kozlov. 2012. “Little Strokes Fell Great Oaks: Minor but Chronic Herbivory Substantially Reduces Birch Growth.” Oikos 121: 2036-43.

Auteurs

Sylvie Berthelot (S)

Biometry and Environmental System Analysis, Albert-Ludwigs-Universität Freiburg, Freiburg, Germany.

Jürgen Bauhus (J)

Chair of Silviculture, Albert-Ludwigs-Universität Freiburg, Freiburg, Germany.

Carsten F Dormann (CF)

Biometry and Environmental System Analysis, Albert-Ludwigs-Universität Freiburg, Freiburg, Germany.

Dominique Gravel (D)

Département de Biologie, Université de Sherbrooke, Sherbrooke, Québec, Canada.

Christian Messier (C)

Département des Sciences Naturelles and Institut des Sciences de la Forêt Tempérée (ISFORT), Université du Québec en Outaouais (UQO), Ripon, Québec, Canada.
Centre d'étude de la Forêt, Université du Québec à Montréal (UQAM), Montréal, Québec, Canada.

Charles A Nock (CA)

Department of Renewable Resources, Earth and Atmospheric Sciences Building, University of Alberta, Edmonton, Alberta, Canada.

Alain Paquette (A)

Centre d'étude de la Forêt, Université du Québec à Montréal (UQAM), Montréal, Québec, Canada.

Peter B Reich (PB)

Department of Forest Resources, University of Minnesota, St. Paul, Minnesota, USA.
Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales, Australia.
Institute for Global Change Biology, University of Michigan, Ann Arbor, Michigan, USA.

Jochen Fründ (J)

Biometry and Environmental System Analysis, Albert-Ludwigs-Universität Freiburg, Freiburg, Germany.

Articles similaires

Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing
Animals Hemiptera Insect Proteins Phylogeny Insecticides
Amaryllidaceae Alkaloids Lycoris NADPH-Ferrihemoprotein Reductase Gene Expression Regulation, Plant Plant Proteins
Drought Resistance Gene Expression Profiling Gene Expression Regulation, Plant Gossypium Multigene Family

Classifications MeSH