Network structure of phytophagous insects associated with Theobroma bicolor (macambo) in an agroforestry system of the Peruvian Amazon

Authors

  • Julio Miguel Grandez-Rios Research Institute of the Peruvian Amazon Author
  • Bruce Leandro Iñape Oroche Research Institute of the Peruvian Amazon Author
  • Walter Santos de Araújo State University of Montes Claros, Department of General Biology Author

DOI:

https://doi.org/10.2478/foecol-2025-0017

Keywords:

biodiversity, connectance, ecological interactions, insect diversity, modularity, specializations

Abstract

Plant-insect interactions play a crucial role in shaping ecosystem structure and dynamics. In the present study, we describe the network structure of phytophagous insects associated with individual Theobroma bicolor in an agroforestry system of the Peruvian Amazon. Network analysis showed higher specialization and modularity than expected by null models, suggesting distinct insect assemblages with unique interactions. At the species level, Chrysomelidae sp. and Antiteuchus tripterus had higher degree and centrality, likely due to their greater mobility and ability to connect different segments of the network. Our findings highlight the high specialization in the phytophagous insect-Theobroma bicolor network. Understanding these interaction patterns can help identify key species and develop management strategies for biodiversity conservation in agroforestry systems.

References

Almeida-NETO, M., Ulrich, W., 2011. A straightforward computational approach for measuring nestedness using quantitative matrices. Environmental Modelling and Software, 26: 173–178. https://doi.org/10.1016/j.envsoft.2010.08.003

Blüthgen, N., Menzel, F., Blüthgen, N., 2006. Measuring specialization in species interaction networks. BMC Ecology, 6: 1–12. https://doi.org/10.1186/1472-6785-6-9

Coral, G.A., Reyna, G.M.T., 2010. Manual de cultivo del Macambo Theobroma bicolor (Humb & Bonpl.) [Cultivation Manual of Macambo Theobroma bicolor (Humb. & Bonpl.)]. IIAP. Iquitos, Perú: Instituto de Investigaciones de la Amazonía Peruana. 44 p. [cit. 2025-04-01]. http://www.iiap.org.pe/upload/publicacion/PUBL534.pdf. (In Spanish).

Dáttilo, W., Marquitti, F.M.D., Guimarães Jr, P.R., Izzo, T.J., 2014. The structure of ant–plant ecological networks: is abundance enough? Ecology, 95: 475–485. https://doi.org/10.1890/12-1647.1

Deheuvels, O., De Waal, L., Bagny-Beilhe, L., 2017. How habitat heterogeneity affects pollinator's communities in cocoa-based agroforestry systems? In Proceedings of the first International Symposium on Cocoa Research ISCR 2017. Lima: ICCO. 5 p. [cit. 2025-04-01]. https://agritrop.cirad.fr/586664/

Delgado, C., Couturier, G., Balcazar, L., Chichipe, A., 2023. Insect pests of Theobroma cacao (Malvaceae) in the Peruvian Amazon. Tropical Agriculture, 100: 110–114.

Delmas, E., Besson, M., Brice, M.H., Burkle, L.A., Riva, G.V.D., Fortin, M.J., Gravel, D., Guimarães, P.R., Hembry, D.H., Newman, E.A., Olesen, J.M., Pires, M.M., Yeakel, J.D., Poisot, T., 2019. Analysing ecological networks of species interactions. Biological Reviews, 94: 16–36. https://doi.org/10.1111/brv.12433

Do, Y., Choi, M.B., 2019. Network analysis for co‐occur-rence of pest insects on host crops. Entomological Research, 49: 35–45. https://doi.org/10.1111/1748-5967.12333

Dormann, C.F., Gruber, B., Fründ, J., 2008. Introducing the bipartite package: Analysing ecological networks. R News, 8: 8–11.

Dormann, C.F., Fründ, J., Blüthgen, N., Gruber, B., 2009. Indices, graphs and null models: analyzing bipartite ecological networks. The Open Journal of Ecology, 2: 7–24.

Elmqvist, T., Folke, C., Nyström, M., Peterson, G., Bengtsson, J., Walker, B., Norberg, J., 2003. Response diversity, ecosystem change, and resilience. Frontiers in Ecology and the Environment, 1: 488–494. https://doi.org/10.1890/1540-9295(2003)001[0488:RDECAR]2.0.CO;2

El-Wakeil, N.E., 2010. Insect economic levels in relation to crop production. Archives of Phytopathology and Plant Protection, 43: 1710–1744. https://doi.org/10.1080/03235400902753584

Fontaine, C., Guimarães JR, P.R., Kéfi, S., Loeuille, N., Memmott, J., Van Der Putten, W.H., Van Veen, F.JF., Thébault, E., 2011. The ecological and evolutionary implications of merging different types of networks. Ecology Letters, 14: 1170–1181. https://doi.org/10.1111/j.1461-0248.2011.01688.x

Fortuna, M.A., Stouffer, D.B., Olesen, J.M., Jordano, P., Mouillot, D., Krasnov, B.R., Poulin, R., Bascompte, J., 2010. Nestedness versus modularity in ecological networks: two sides of the same coin? Journal of Animal Ecology, 79: 811–817. https://doi.org/10.1111/j.1365-2656.2010.01688.x

Grilli, J., Rogers, T., Allesina, S., 2016. Modularity and stability in ecological communities. Nature Communications, 7: 12031. https://doi.org/10.1038/ncomms12031

Harterreiten-Souza, E.S., Togni, P.H.B., Pires, C.S.S., Sujii, E.R., 2014. The role of integrating agroforestry and vegetable planting in structuring communities of herbivorous insects and their natural enemies in the Neotropical region. Agroforestry Systems, 88: 205–219. https://doi.org/10.1007/s10457-013-9666-1

Jankielsohn, A., 2018. The importance of insects in agricul- tural ecosystems. Advances in Entomology, 6: 62–73.

Jordano, P., 2016. Sampling networks of ecological interactions. Functional Ecology, 30: 1883–1893. https://doi.org/10.1111/1365-2435.12763

Lagneaux, E., Andreotti, F., Neher, C.M., 2021. Cacao, copoazu and macambo: Exploring Theobroma diversity in smallholder agroforestry systems of the Peruvian Amazon. Agroforestry Systems, 95: 1359–1368. https://doi.org/10.1007/s10457-021-00610-0

Lewinsohn, T.M., Prado, P.I., Jordano, P., Bascompte, J., Olesen, J.M., 2006. Structure in plant–animal interaction assemblages. Oikos, 113: 174–184. https://doi.org/10.1111/j.0030-1299.2006.14583.x

Marengo, J.A., 1998. Climatologia de la zona de Iquitos, Peru [Climatology of the Iquitos Region, Peru]. In Kalliola, R., Paintan, S.F., (eds). Geoecologia y desarrollo amazónico: estudio integrado en la zona de Iquitos, Peru. Turku: Turun Yliopisto, p. 35–57. (In Spanish).

Melo, A.S., Paz-Neto, A. A., Melo, J.W.S., Gondim-Junior, M.G.C., 2024. Interspecific interaction network of mites associated with mango trees. Experimental and Applied Acarology, 93: 353–367. https://doi.org/10.1007/s10493-024-00936-1

Novotný, V., Basset, Y., 2000. Rare species in communities of tropical insect herbivores: pondering the mystery of singletons. Oikos, 89: 564–572. https://doi.org/10.1034/j.1600-0706.2000.890316.x

Olesen, J.M., Bascompte, J., Dupont, Y.L., Jordano, P.,2007. The modularity of pollination networks. Proceedings of the National Academy of Sciences, 104: 19891–19896. https://doi.org/10.1073/pnas.0706375104

Oliveira, J.B.B.S., Faria, M.L., Borges, M.A., Fagundes, M., Araújo, W.S., 2020. Comparing the plant–herbivore network topology of different insect guilds in Neotropical savannas. Ecological Entomology, 45: 406–415. https://doi.org/10.1111/een.12808

Pinho, B.X., Dáttilo, W., Leal, I.R., 2017. Structural breakdown of specialized plant-herbivore interaction networks in tropical forest edges. Global Ecology and Conservation, 12: 1–8. https://doi.org/10.1016/j.gecco.2017.08.007

Power, A.G., 2010. Ecosystem services and agriculture: tradeoffs and synergies. Philosophical Transactions of the Royal Society B: Biological Sciences, 365: 2959–2971. https://doi.org/10.1098/rstb.2010.0143

Shanker, C., Solanki, K.R., 2000. Agroforestry: an eco-friendly land-use system for insect management. Outlook on Agriculture, 29: 91–96. https://doi.org/10.5367/000000000101293

Tineo, D., Calderon, M.S., Maicelo, J.L., Oliva, M., Huamán-Pilco, Á.F., Ananco, O., Bustamante, D.E., 2024. Characterization and phylogenetic analysis of the complete plastid genome of Theobroma bicolor (Malvaceae) from Peru. Mitochondrial DNA Part B, 9: 227–232. https://doi.org/10.1080/23802359.2024.2310134

Torralba, M., Fagerholm, N., Burgess, P.J., Moreno, G., Plieninger, T., 2016. Do European agroforestry systems enhance biodiversity and ecosystem services? A meta-analysis. Agriculture, Ecosystems and Environment, 230: 150–161. https://doi.org/10.1016/j.agee.2016.06.002

Tscharntke, T., Klein, A.M., Kruess, A., Steffan‐Dewenter, I., Thies, C., 2005. Landscape perspectives on agricultural intensification and biodiversity–ecosystem service management. Ecology Letters, 8: 857–874. https://doi.org/10.1111/j.1461-0248.2005.00782.x

Windsor, F.M., Armenteras, D., Assis, A.P.A., Astegiano, J., Santana, P.C., Cagnolo, L., Carvalheiro, L.G., Emary, C., Fort, H., Gonzalez, X.I., Kitson, J.J.N., Lacerda, A.C.F., Lois, M., Márquez-Velásquez, V., Miller, K.E., Monasterolo, M., Omacini, M., Maia, K.P., Palacios, T.P., Pocock, M.J.O., Poggio, S.L., Varassin, I.G., Vázquez, D.P., Tavella, J., Rother, D.C., Devoto, M., Guimarães, P.R., Evans, D.M., 2022. Network science: Applications for sustainable agroecosystems and food security. Perspectives in Ecology and Conservation, 20: 79–90. https://doi.org/10.1016/j.pecon.2022.03.001

Zahra, S., Jorge, L., Dáttilo, W., Klimeš, P., Ferreira, P.D.L., Christianini, A., Nunes-Freitas, A.P., Laviski, B.F.S., Wang, B., Emer, C., Lara, C., Castillo-Guevara, C., Gomez, C., Corro, E., Lenc, J., Falcão, J., Tavella, J., Cagnolo, L., Pizo, M.A., Cuautle, M., Tahadlova, M., STAAB, M., Mottl, O., Miranda, N.P., Oliveira, P., Butterill, P.T., Antoniazzi, R., Xing, S., Izzo, T., Novotny, V., Fayle, T., 2024. Ant-plant specialisation depends on network type, but not disturbance, elevation, or latitude. Authorea, 6 May. [cit. 2025-04-01]. https://doi.org/10.22541/au.171500704.45910925/v1

Downloads

Published

2025-07-23

Issue

Section

Articles