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Variation in defensive traits against herbivores of native and invasive populations of Carpobrotus edulis

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Abstract

The Enemy Release Hypothesis (ERH) predicts that the escape from natural enemies, such as specialist herbivores, may explain the invasiveness of some invasive alien plants, maximizing their investment in growth and reproduction. This release from natural enemies might decrease the investment in expensive defense mechanisms (i.e., digestibility reducers) against the attack of specialist enemies, whilst increasing the investment in defenses (i.e., cheap toxins) and tolerance against the attack of generalist herbivores, as exposed by the Shifting Defense Hypothesis (SDH). To test this, we conducted a greenhouse experiment to compare morphological and physiological traits of Carpobrotus edulis, collected in its native (South Africa) and introduced (Chile and Spain) ranges, attacked by the generalist spittlebug Philaenus spumarius and the specialist scale insect Pulvinariella mesembryanthemi. Our results do not support the ER and SD hypotheses. We found that C. edulis plants collected from native and introduced ranges showed no significant differences in growth and defensive compounds studied for both controls and those plants under attack by the generalist P. spumarius (i.e., showing no increase in biomass or changes in biochemical defenses). In contrast, the specialist herbivore P. mesembryanthemi induced the production of total phenols and tannins and reduced the growth and survival of C. edulis plants. Overall, we found strong evidence that C. edulis is negatively affected by the attack of its specialist herbivore, but not by that of generalist herbivore, regardless of origin. The observed tolerance to generalist herbivores suggests the intriguing possibility of trait selection, allowing C. edulis plants to tolerate generalist herbivores more than specialists.

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The datasets generated during and/or analyzed during the current study are available in the FigShare repository. https://doi.org/10.6084/m9.figshare.14604486.v1

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Acknowledgements

We are grateful to Desika Moodley for their valuable comments on the manuscript and English editing. This work was carried out within the framework of the project “Retos en la gestión de la planta invasora Carpobrotus edulis. Variabilidad fenotípica y cambios en la relación suelo-planta durante el proceso de invasion” (in Spanish), Reference CGL2013-48885-C2-1-R, funded by the Ministry of Economy and Competitiveness (Spanish Government). JR acknowledges financial support from the European Union NextGenerationEU and “Plan de Recuperación, Transformación y Resiliencia” awarded by the Ministry of Universities and granted by the Universidade de Vigo (UP2021-046) through the Margarita Salas program. JR and AN acknowledge funding from the Czech Science Foundation (Project No. 19-13142S and EXPRO Grant No. 19-28807X); and the Czech Academy of Sciences (long-term research development project No. RVO 67985939). AP was funded by CONICYT PIA AFB-170008. We sincerely thank the constructive and very helpful comments provided by the two anonymous reviewers that substantially improved the final version of the manuscript.

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JR designed the methodology and led the writing of the manuscript; JR and GS conceived the ideas; JR, AN, GS, AP and LG collected the seeds, and JR the insects; JR performed the experiment, collected, and analyzed the data. All authors contributed to the drafts, agreed on the content and gave final approval for publication.

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Correspondence to Jonatan Rodríguez.

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The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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Rodríguez, J., Novoa, A., Sotes, G. et al. Variation in defensive traits against herbivores of native and invasive populations of Carpobrotus edulis. Biol Invasions 25, 1149–1164 (2023). https://doi.org/10.1007/s10530-022-02970-9

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  • DOI: https://doi.org/10.1007/s10530-022-02970-9

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