Abstract
Species contribute differently to the structure and stability of networks of interacting species. However, species contributions to the importance of other species is usually neglected, thus limiting our understanding of species dynamics beyond the general network structure. We combined knowledge on diversity effects on focal species and network ecology to analyze the influence of plants and herbivores on big-leaf mahogany's (Swietenia macrophylla) importance in the plant–herbivore network. To this end, we built interaction networks using information from a large-scale tree diversity experiment and performed computer simulations of species removal with redistribution of interactions. We compared the importance of big-leaf mahogany in the observed networks to simulated networks where we removed: (a) tree species with similar beetle assemblages to mahogany, (b) the most interconnected (core) tree species and (c) the core beetle species. Removal of the core and similar tree species increased the importance of mahogany, whereas eliminating core beetle species decreased it. Interestingly, the effect of core tree species on mahogany’s importance was mediated by core beetles (R2 = 0.46). Neither tree nor core beetle species’ effects were contingent on tree species richness or abundance. These results indicate that highly connected tree and herbivore species jointly determine the role of mahogany in the plant–herbivore network. Likewise, these results provide insight into the effect of tree species composition and highly interactive herbivores in shaping the role of species in the herbivore network.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
All data produced from this study are provided in this manuscript as supplementary material.
Code availability
Code can be consulted on the supplementary material.
References
Abdala-Roberts L, Mooney KA, Quijano-Medina T et al (2015) Comparison of tree genotypic diversity and species diversity effects on different guilds of insect herbivores. Oikos 124:1527–1535. https://doi.org/10.1111/oik.02033
Abdala-Roberts L, González-Moreno A, Mooney KA et al (2016) Effects of tree species diversity and genotypic diversity on leafminers and parasitoids in a tropical forest plantation. Agric For Entomol 18:43–51. https://doi.org/10.1111/afe.12132
Barbosa P, Hines J, Kaplan I et al (2009) Associational resistance and associational susceptibility: having right or wrong neighbors. Annu Rev Ecol Evol Syst 40:1–20. https://doi.org/10.1146/annurev.ecolsys.110308.120242
Barwell LJ, Isaac NJB, Kunin WE (2015) Measuring β-diversity with species abundance data. J Anim Ecol 84:1112–1122. https://doi.org/10.1111/1365-2656.12362
Bascompte J, Jordano P, Melian CJ, Olesen JM (2003) The nested assembly of plant-animal mutualistic networks. Proc Natl Acad Sci U S A 100:9383–9387. https://doi.org/10.1073/pnas.1633576100
Bascompte J, Jordano P, Olesen MJ (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433. https://doi.org/10.1126/science.1123412
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Bertheau C, Brockerhoff EG, Roux-Morabito G et al (2010) Novel insect-tree associations resulting from accidental and intentional biological ‘invasions’: a meta-analysis of effects on insect fitness. Ecol Lett 13:506–515. https://doi.org/10.1111/j.1461-0248.2010.01445.x
Bird G, Kaczvinsky C, Wilson AE, Hardy NB (2019) When do herbivorous insects compete? A phylogenetic meta-analysis. Ecol Lett 22:875–883. https://doi.org/10.1111/ele.13245
Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecol 6:9. https://doi.org/10.1186/1472-6785-6-9
Boege K, Barton KE, Dirzo R (2011). In: Meinzer FC, Lachenbruch B, Dawson TE (eds) Influence of tree ontogeny on plant-herbivore interactions BT: size- and age-related changes in tree structure and function. Springer, Netherlands, Dordrecht, pp 193–214
Bramon Mora B, Shin E, CaraDonna PJ, Stouffer DB (2020) Untangling the seasonal dynamics of plant-pollinator communities. Nat Commun 11:4086. https://doi.org/10.1038/s41467-020-17894-y
Brosi BJ, Briggs HM (2013) Single pollinator species losses reduce floral fidelity and plant reproductive function. Proc Natl Acad Sci USA 110:13044–13048. https://doi.org/10.1073/pnas.1307438110
Campos-Navarrete MJ, Abdala-Roberts L, Munguía-Rosas MA, Parra-Tabla V (2015) Are tree species diversity and genotypic diversity effects on insect herbivores mediated by ants? PLoS ONE 10:e0132671. https://doi.org/10.1371/journal.pone.0132671
Campos-Navarrete MJ, Munguía-Rosas MA, Abdala-Roberts L et al (2015) Effects of tree genotypic diversity and species diversity on the arthropod community associated with big-leaf mahogany. Biotropica 47:579–587. https://doi.org/10.1111/btp.12250
Carvalheiro LG, Buckley YM, Ventim R et al (2008) Apparent competition can compromise the safety of highly specific biocontrol agents. Ecol Lett 11:690–700. https://doi.org/10.1111/j.1461-0248.2008.01184.x
Castagneyrol B, Jactel H, Vacher C et al (2014) Effects of plant phylogenetic diversity on herbivory depend on herbivore specialization. J Appl Ecol 51:134–141. https://doi.org/10.1111/1365-2664.12175
Chao A, Chazdon RL, Colwell RK, Shen T-J (2006) Abundance-based similarity indices and their estimation when there are unseen species in samples. Biometrics 62:361–371. https://doi.org/10.1111/j.1541-0420.2005.00489.x
CITES (2003) Enforcing the provisions of the convection concerning trade in Swietenia macrophylla. CITES Secretariat, Geneva
Coux C, Rader R, Bartomeus I, Tylianakis JM (2016) Linking species functional roles to their network roles. Ecol Lett 19:762–770. https://doi.org/10.1111/ele.12612
Dáttilo W, Guimarães PR, Izzo TJ (2013) Spatial structure of ant–plant mutualistic networks. Oikos 122:1643–1648. https://doi.org/10.1111/j.1600-0706.2013.00562.x
Delmas E, Besson M, Brice M-H et al (2019) Analysing ecological networks of species interactions. Biol Rev 94:16–36. https://doi.org/10.1111/brv.12433
Dupont YL, Olesen JM (2009) Ecological modules and roles of species in heathland plant–insect flower visitor networks. J Anim Ecol 78:346–353. https://doi.org/10.1111/j.1365-2656.2008.01501.x
Endara M-J, Coley PD, Ghabash G et al (2017) Coevolutionary arms race versus host defense chase in a tropical herbivore–plant system. Proc Natl Acad Sci USA 114:E7499–E7505. https://doi.org/10.1073/pnas.1707727114
Erwin TL (1982) Tropical forests: their richness in Coleoptera and other species. Coleopt Bull 36:74–75
Fort H, Vázquez DP, Lan BL (2016) Abundance and generalisation in mutualistic networks: solving the chicken-and-egg dilemma. Ecol Lett 19:4–11. https://doi.org/10.1111/ele.12535
García-Robledo C, Kuprewicz EK, Baer CS et al (2020) The Erwin equation of biodiversity: from little steps to quantum leaps in the discovery of tropical insect diversity. Biotropica 52:590–597. https://doi.org/10.1111/btp.12811
Gilbert GS, Magarey R, Suiter K, Webb CO (2012) Evolutionary tools for phytosanitary risk analysis: phylogenetic signal as a predictor of host range of plant pests and pathogens. Evol Appl 5:869–878. https://doi.org/10.1111/j.1752-4571.2012.00265.x
González-Castro A, Yang S, Nogales M, Carlo TA (2012) What determines the temporal changes of species degree and strength in an oceanic island plant-disperser network? PLoS ONE 7:e41385. https://doi.org/10.1371/journal.pone.0041385
Grogan J, Blundell AG, Landis RM et al (2010) Over-harvesting driven by consumer demand leads to population decline: big-leaf mahogany in South America. Conserv Lett 3:12–20. https://doi.org/10.1111/j.1755-263X.2009.00082.x
Grossman JJ, Cavender-Bares J, Reich PB et al (2019) Neighborhood diversity simultaneously increased and decreased susceptibility to contrasting herbivores in an early stage forest diversity experiment. J Ecol 107:1492–1505. https://doi.org/10.1111/1365-2745.13097
Hackett TD, Sauve AMC, Davies N et al (2019) Reshaping our understanding of species’ roles in landscape-scale networks. Ecol Lett 22:1367–1377. https://doi.org/10.1111/ele.13292
Hedges LV (2007) Effect sizes in cluster-randomized designs. J Educ Behav Stat 32:341–370. https://doi.org/10.3102/1076998606298043
Heimonen K, Lwanga JS, Mutanen M et al (2013) Spatial and temporal variation in community composition of herbivorous insects on Neoboutonia macrocalyx in a primary tropical rain forest. J Trop Ecol 29:229–241
Hothorn T, Bretz F, Westfall P (2008) Simultaneous Inference in General Parametric Models. Biometrical J 50:346–363. https://doi.org/10.1002/bimj.200810425
Ings TC, Montoya JM, Bascompte J et al (2009) Review: Ecological networks: beyond food webs. J Anim Ecol 78:253–269. https://doi.org/10.1111/j.1365-2656.2008.01460.x
Jactel H, Brockerhoff EG (2007) Tree diversity reduces herbivory by forest insects. Ecol Lett 10:835–848. https://doi.org/10.1111/j.1461-0248.2007.01073.x
Jordano P (2016) Sampling networks of ecological interactions. Funct Ecol 30:1883–1893. https://doi.org/10.1111/1365-2435.12763
Junker RR, Höcherl N, Blüthgen N (2010) Responses to olfactory signals reflect network structure of flower-visitor interactions. J Anim Ecol 79:818–823. https://doi.org/10.1111/j.1365-2656.2010.01698.x
Kim TN, Underwood N (2015) Plant neighborhood effects on herbivory: damage is both density and frequency dependent. Ecology 96:1431–1437. https://doi.org/10.1890/14-1097.1
Lewinsohn TM, Inácio Prado P, Jordano P et al (2006) Structure in plant–animal interaction assemblages. Oikos 113:174–184. https://doi.org/10.1111/j.0030-1299.2006.14583.x
Luviano N, Villa-Galaviz E, Boege K et al (2018) Hurricane impacts on plant-herbivore networks along a successional chronosequence in a tropical dry forest. For Ecol Manage 426:158–163. https://doi.org/10.1016/j.foreco.2017.09.011
Macfadyen S, Cunningham SA, Costamagna AC, Schellhorn NA (2012) Managing ecosystem services and biodiversity conservation in agricultural landscapes: are the solutions the same? J Appl Ecol 49:690–694. https://doi.org/10.1111/j.1365-2664.2012.02132.x
Maia KP, Vaughan IP, Memmott J (2019) Plant species roles in pollination networks: an experimental approach. Oikos 128:1446–1457. https://doi.org/10.1111/oik.06183
Martín González AM, Dalsgaard B, Olesen JM (2010) Centrality measures and the importance of generalist species in pollination networks. Ecol Complex 7:36–43. https://doi.org/10.1016/j.ecocom.2009.03.008
Memmott J, Waser NM, Price MV (2004) Tolerance of pollination networks to species extinctions. Proc Biol Sci 271:2605–2611. https://doi.org/10.1098/rspb.2004.2909
Miele V, Ramos-Jiliberto R, Vázquez DP (2020) Core–periphery dynamics in a plant–pollinator network. J Anim Ecol 89:1670–1677. https://doi.org/10.1111/1365-2656.13217
Morrison BML, Brosi BJ, Dirzo R (2020) Agricultural intensification drives changes in hybrid network robustness by modifying network structure. Ecol Lett 23:359–369. https://doi.org/10.1111/ele.13440
Negreros Castillo P, Cámara Cabrales LC, Devall MS et al (2014) Silvicultura de las selvas de caoba en Quintana Roo, México: criterios y recomendaciones. Comisión Nacional Forestal, Mexico
Norghauer JM, Grogan J, Malcolm JR, Felfili JM (2010) Long-distance dispersal helps germinating mahogany seedlings escape defoliation by a specialist caterpillar. Oecologia 162:405–412. https://doi.org/10.1007/s00442-009-1476-9
Nuwagaba S, Zhang F, Hui C (2017) Robustness of rigid and adaptive networks to species loss. PLoS ONE 12:e0189086. https://doi.org/10.1371/journal.pone.0189086
Oksanen J, Blanchet FG, Friendly M, et al (2019) vegan: Community ecology package. R package version 2.5–4.
Pennington TD, Sarukhán J (2005) Árboles tropicales de México: manual para la identificación de las principales especies. UNAM, Mexico
Pinheiro RBP, Felix GMF, Dormann CF, Mello MAR (2019) A new model explaining the origin of different topologies in interaction networks. Ecology 100:e02796. https://doi.org/10.1002/ecy.2796
Pocock MJO, Johnson O, Wasiuk D (2011) Succinctly assessing the topological importance of species in flower-pollinator networks. Ecol Complex 8:265–272. https://doi.org/10.1016/j.ecocom.2011.06.003
Quinto J, Martínez-Falcón AN, Murillo-Pacheco JI et al (2021) Diversity patterns of tropical epigeal beetle assemblages associated with monoculture and polyculture plantations with big-leaf mahogany. Neotrop Entomol 50:551–561. https://doi.org/10.1007/s13744-021-00870-6
Quinto J, Díaz-Castelazo C, Rico-Gray V et al (2022) Short-term temporal patterns in herbivore beetle assemblages in polyculture neotropical forest plantations. Neotrop Entomol 51:199–211. https://doi.org/10.1007/s13744-021-00933-8
R Core Team (2020) R: a language and environment for statistical computing. R Foundation of Statistical Computing, Vienna
Sanders D, Thébault E, Kehoe R, Frank van Veen FJ (2018) Trophic redundancy reduces vulnerability to extinction cascades. Proc Natl Acad Sci USA 115:2419–2424. https://doi.org/10.1073/pnas.1716825115
Schoonhoven LM, van Loon JJA, Dicke M (2006) Insect-plant biology, 2nd edn. Oxford University Press, Oxford
Schuldt A, Assmann T, Bruelheide H et al (2014) Functional and phylogenetic diversity of woody plants drive herbivory in a highly diverse forest. New Phytol 202:864–873. https://doi.org/10.1111/nph.12695
Solé RV, Montoya JM (2001) Complexity and fragility in ecological networks. Proc R Soc Lond. B Biol Sci 268:2039–2045. https://doi.org/10.1098/rspb.2001.1767
Tahvanainen JO, Root RB (1972) The influence of vegetational diversity on the population ecology of a specialized herbivore, Phyllotreta cruciferae (Coleoptera: Chrysomelidae). Oecologia 10:321–346. https://doi.org/10.1007/BF00345736
Vázquez DP, Melián CJ, Williams NM et al (2007) Species abundance and asymmetric interaction strength in ecological networks. Oikos 116:1120–1127. https://doi.org/10.1111/j.0030-1299.2007.15828.x
Verwer C, Peña-Claros M, Van Der Staak D et al (2008) Silviculture enhances the recovery of overexploited mahogany Swietenia macrophylla. J Appl Ecol 45:1770–1779. https://doi.org/10.1111/j.1365-2664.2008.01564.x
Yguel B, Bailey R, Tosh ND et al (2011) Phytophagy on phylogenetically isolated trees: why hosts should escape their relatives. Ecol Lett 14:1117–1124. https://doi.org/10.1111/j.1461-0248.2011.01680.x
Zuur AF, Ieno EN, Walker NJ et al (2009) Mixed effects models and extensions in ecology with R. Springer-Verlag, New York
Acknowledgements
We are thankful to INIFAP who provided logistic accommodations and infrastructure for the establishment of the experiment, subsequent sampling, and maintenance. We would like to thank to R. Anderson, A.R. Cline, P. Cifuentes, M.L. Gimmel, T.L. Grzymala, R. Jones, P. Leblanc, S. López, G.M. Rodríguez Mirón, V.H. Toledo and M.L. Zurita García for their help with the identifications. We are grateful to N. Celaya, E. Fonseca, A. González, V. Hernández, D. Marrufo, D. Medellín, P. Medina, R. Mena, O. Orozco, T. Quijano, N. Salinas, V. Solís, P. Téllez and J. Tun for field assistance. We thank T. Timberlake for proof reading the manuscript. We thank the reviewers for their valuable suggestions and comments that greatly improved the quality of the manuscript.
Funding
CONACyT grant awarded to VPT and LAR (128856).
Author information
Authors and Affiliations
Contributions
EVG formulated the idea and analyzed the data. LA-R and VP-T conceived and designed the experimental site. JQ and MJC-N designed and conducted fieldwork. EVG wrote the manuscript with input from LA-R and VP-T; other authors provided editorial advice.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that there is no conflict of interest.
Ethical approval
“All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.”
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling Editor: Heikki Hokkanen.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Villa-Galaviz, E., Abdala-Roberts, L., Quinto, J. et al. Neighboring plants and core herbivores determine the importance of Swietenia macrophylla in the plant–herbivore network. Arthropod-Plant Interactions 16, 387–399 (2022). https://doi.org/10.1007/s11829-022-09906-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-022-09906-z