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How is leaf herbivory related to agriculture? Insights from the Mexican center of crop origin

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Abstract

Although insect herbivory is thought to be higher in agroecosystems compared to natural ecosystems, direct evidence on how agriculture itself has impacted herbivory remains scarce. To understand the effects of agriculture, or the cultivation of domesticated crops, over higher trophic levels, it is necessary to compare cultivated crops and their wild counterparts in centers of origin. In such regions, insect herbivores have a shared history of interacting with wild host plants prior to crop domestication and cultivation. However, most studies evaluating the impacts of agriculture on herbivory have been conducted in geographic regions where crops have been introduced. Here, we studied how insect herbivory is related to agriculture in Mexico, which is part of the Mesoamerican center of origin. We focused on patterns of leaf herbivory across four Mexican crops (squash, beans, maize, and husk tomatoes). We tested if total leaf herbivory, as well as the composition and dominance of different types of damage caused by leaf-feeding insects, differed between domesticated crops and their wild counterparts. Overall, we found that the relationship between agriculture and leaf herbivory depends on the observed crop. Compared to their wild ancestors (or wild relatives), leaf herbivory was higher in squash and maize, lower in husk tomatoes, and similar in beans. We also found that, due to differences in damaged area and/or shifts in dominance, damage compositions varied in squash, maize, and husk tomatoes. Therefore, our findings reinforce the idea that crop resistance against herbivory varies depending on the plant species and herbivore under study.

Resumen

Aunque se cree que la herbivoría causada por insectos es mayor en los agroecosistemas en comparación con los ecosistemas naturales, la evidencia directa sobre cómo la agricultura per se ha impactado la herbivoría sigue siendo escasa. Para entender los efectos de la agricultura, o el cultivo de plantas domesticadas, sobre niveles tróficos superiores, es importante comparar cultivos domesticados y sus contrapartes silvestres creciendo en centros de origen. En estas regiones, los insectos herbívoros comparten una historia evolutiva con las plantas silvestres desde antes de la domesticación y la cultivación. Sin embargo, la mayoría de los estudios que evalúan los impactos de la agricultura sobre la herbivoría se han realizado en regiones geográficas donde los cultivos han sido introducidos. Aquí, estudiamos cómo la herbivoría de hojas causada por insectos se relaciona con la agricultura en México; parte del centro de origen mesoamericano. Nos enfocamos en los patrones de herbivoría de hojas de cuatro cultivos mexicanos (calabazas, frijoles, maíz y tomates de cáscara). Evaluamos si la herbivoría total en las hojas, así como las composiciones y dominancias de diferentes tipos de daños causados por insectos devoradores de hojas, difieren entre cultivos y sus contrapartes silvestres. En general, encontramos que la relación entre laagricultura y la herbivoría de hojas depende del cultivo observado. En comparación con sus ancestros silvestres (o parientes silvestres), la herbivoría de hojas fue mayor en calabazas y maíz, menor en tomates de cáscara, y similar en frijoles. También encontramos que, debido a diferencias en áreas dañadasy/o cambios en dominancia, la composición de daños varió en calabazas, maíz y tomates de cáscara. Por ende, nuestros hallazgos refuerzan la idea de que la resistencia de los cultivos a la herbivoría varía dependiendo de la especie de planta y herbívoro bajo estudio.

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The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

This work was possible due to help in the field and/or in the laboratory provided by A.C. Villalobos-Hau, D. Morales-Villegas, F.J. López, H. Morales, I. Sandoval, J.A. Pérez-Meda, J.J. Adame, J. Fernando, J. Sánchez, L. Guzmán, M. Aguiano, N. Gálvez, O. Rojo-Nava and P. Rodríguez-Juárez. We are profoundly grateful to the dozens of indigenous and farmer communities who welcomed us, provided access to their private lands, helped us find crop wild relatives, and shared their knowledge on local flora and agricultural management. Finally, we are also thankful for the text revisions by A. Campbell, B. Christensen, E. Bueno, E. von Wettberg, J. Gunn and R. Carrera-Martínez, and the suggestions of multiple anonymous reviewers that greatly improved the manuscript. All samplings were conducted following the Secretaría de Medio Ambiente y Recursos Naturales (SEMARNAT-México) sampling permit: SGPA-DGGFS-712-1995-18 administered by AW.

Funding

Financial support was provided by a City Market Co-op Patronage Seedling Grant, Gund Institute for the Environment Catalyst Award, and a Conservation, Food & Health Foundation granted to YHC. In addition, JRA was supported by a Sigma Xi award (G2018031596099894) and an UVM Food System Research Center Fellowship.

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Correspondence to Jorge Ruiz-Arocho.

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Ruiz-Arocho, J., González-Salas, R., LeMay, G. et al. How is leaf herbivory related to agriculture? Insights from the Mexican center of crop origin. Arthropod-Plant Interactions 18, 89–104 (2024). https://doi.org/10.1007/s11829-023-10019-4

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