Hostname: page-component-669899f699-8p65j Total loading time: 0 Render date: 2025-04-25T11:33:34.944Z Has data issue: false hasContentIssue false

Phenotypic plasticity and insect herbivory of trees in contrasting light environments in a Mexican rainforest

Published online by Cambridge University Press:  20 November 2024

Daniel A. Cadena-Zamudio*
Affiliation:
Red de Biología Evolutiva, Instituto de Ecología A.C, Xalapa, Veracruz, México
Roger Guevara
Affiliation:
Red de Biología Evolutiva, Instituto de Ecología A.C, Xalapa, Veracruz, México
Betsabé Ruiz-Guerra
Affiliation:
Red de Interacciones Multitróficas, Instituto de Ecología A.C, Xalapa, Veracruz, México
*
Corresponding author: Daniel A. Cadena-Zamudio; Email: [email protected]

Abstract

Contrasting light environments in rainforests generates changes in the characteristics of the leaves and in the herbivore community. In the present study, we carried out a reciprocal transplant experiment under natural conditions to determine the plasticity of leaf characteristics of plant species that grow in contrasting light environments in a Neotropical forest. We further explored the relationship between these traits and insect herbivory. We found that six woody species differ markedly in the phenotypic plasticity of leaf features. The specific leaf area, chlorophyll content, carbon content, nitrogen content, and leaf thickness of the most light-demanding species were highest in gaps, but their carbon/nitrogen ratios were higher under closed canopies. The herbivores were more abundant in gaps (5.9%–14.8%) than under closed canopy habitats (3.4%–6.1%) and seemingly associated to the plasticity of the leaf traits. We observed 47% more herbivores in gaps than under closed canopies. Our results suggest that the phenotypic plasticity of leaf traits depends on the identity of the plant species and its wood density, while herbivory seems to be affected by plant defence, low nutritional quality, or herbivore tolerance.

Type
Research Article
Copyright
© The Author(s), 2024. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Adams, WW III, Stewart, JJ, Polutchko, SK, Cohu, CM, Muller, O and Demmig-Adams, B (2023) Foliar phenotypic plasticity reflects adaptation to environmental variability. Plants 12, 2041.CrossRefGoogle ScholarPubMed
Adler, PB, Salguero-Gómez, R, Compagnoni, A, Hsu, JS, Ray-Mukherjee, J, Mbeau-Ache, C and Franco, M (2014) Functional traits explain variation in plant life history strategies. Proceedings of the National Academy of Sciences 111, 740745.CrossRefGoogle ScholarPubMed
Agrawal, AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294, 321326. https://doi:10.1126/science.1060701 CrossRefGoogle ScholarPubMed
Agrawal, AA and Fishbein, M (2006) Plant defense syndromes. Ecology 87, S132S149.CrossRefGoogle ScholarPubMed
Baraza, E, Zamora, R and Hódar, JA (2010) Species-specific responses of tree saplings to herbivory in contrasting light environments: an experimental approach. Écoscience 17, 156165.CrossRefGoogle Scholar
Boege, K and Dirzo, R (2004) Intraspecific variation in growth, defense and herbivory in Dialium guianense (Caesalpiniaceae) mediated by edaphic heterogeneity. Vegetation 175, 5969.Google Scholar
Buck, M, Woodley, NE, Borkent, A, Wood, DM, Pape, Th, Vockeroth, JR, Michelsen, V and Marshall, SA (2009) Key to Diptera Families - Adults. In Brown, BV, Borkent, A, Cumming, JM. (eds), Manual of Central American Diptera Vol 1. Ottawa: NRC Research Press, pp. 95144.Google Scholar
Chave, J, Coomes, D, Jansen, S, Lewis, SL, Swenson, NG and Zanne, AE (2009) Towards a worldwide wood economics spectrum. Ecology Letters 12, 351366.CrossRefGoogle ScholarPubMed
Cibrián, TD, Méndez, JT, Campos, MR, Yates, BHO III and Flores, JEL (1995) Insectos Forestales de México/Forest Insects of México. Universidad Autónoma de Chapingo. SARH Subsecretaria Forestal y de Fauna Silvestre, México. USDA, Forest Service, Natural Resources Canada. North American Forestry Commission, FAO. Pub 6. (pp. 453).Google Scholar
Coley, PD and Barone, JA (1996) Herbivory and plant defenses in tropical forests. Annual Review of Ecology and Systematics 27, 305335.CrossRefGoogle Scholar
Cornejo-Tenorio, G, Manríquez, GI and Colín, SS (2019) Flora de Los Tuxtlas: guía ilustrada. Universidad Nacional Autónoma de México.Google Scholar
De la Cruz, M and Dirzo, R (1988) A survey of the standing levels of herbivory in seedlings from a Mexican rain forest. Biotropica 19, 98106.CrossRefGoogle Scholar
de Mello Prado, R and da Silva, GP (2017) Ecological response to global change: Changes in C: N: P stoichiometry in environmental adaptations of plants. Plant Ecology: Traditional Approaches to Recent Trends, 147.Google Scholar
Delph, LF (2017) The study of local adaptation: a thriving field of research. Journal of Heredity 109, 12. https://doi:10.1093/jhered/esx099 CrossRefGoogle Scholar
DeWitt, TJ and Scheiner, SM (2004) Phenotypic Variation from Single Genotypes: A Primer. In DeWitt, TJ and Samuel, MS (eds), Phenotypic Plasticity: Functional and Conceptual Approaches. New York, USA: Oxford Academic Press, pp. 19.CrossRefGoogle Scholar
Dirzo, R and Domínguez, CA (1995) Plant–herbivore interactions in Mesoamerican tropical dry forests. In Bullock, S. H., Mooney, H. A. and Medina, E. (eds), Seasonal dry tropical forests. Cambridge, UK: Cambridge University Press, pp. 304325 CrossRefGoogle Scholar
Dray, S, Chessel, D and Thioulouse, J (2003) Co-inertia analysis and the linking of ecological data table. Ecology 84, 30783089.CrossRefGoogle Scholar
Dupuy, JM and Chazdon, RL (2008) Interacting effects of canopy gap, understory vegetation and leaf litter on tree seedling recruitment and composition in tropical secondary forests. Forest Ecology and Management 255, 37163725 CrossRefGoogle Scholar
Falster, DS, Duursma, RA and FitzJohn, RG (2018) How functional traits influence plant growth and shade tolerance across the life cycle. Proceedings of the National Academy of Sciences 115, E6789E6798. https://doi.org/10.1073/pnas.171404411CrossRefGoogle ScholarPubMed
Gianoli, E and Salgado-Luarte, C (2017) Tolerance to herbivory and the resource availability hypothesis. Biology Letters 13, 20170120.CrossRefGoogle ScholarPubMed
Gianoli, E, Salgado-Luarte, C and Escobedo, VM (2023) Shade tolerance and the relationship between herbivory and light availability. International Journal of Plant Sciences 184, 519524.CrossRefGoogle Scholar
Heo, M and Gabriel, KR (1997) A permutation test of association between configurations by means of the RV coefficient. Communications in Statistics - Simulation and Computation 27, 843856.Google Scholar
Hoch, G, Richter, A and Körner, C (2003) Non-structural carbon compounds in temperate forest trees. Plant, Cell & and Environment 26, 10671081.CrossRefGoogle Scholar
Karolewski, P, Giertych, MJ, Żmuda, M, Jagodziński, AM and Oleksyn, J (2013) Season and light affect constitutive defenses of understory shrub species against folivorous insects. Acta Oecologica 53, 1932.CrossRefGoogle Scholar
King, DA, Davies, SJ, Tan, S and Noor, NS (2006) The role of wood density and stem support costs in the growth and mortality of tropical trees. Journal of Ecology 94, 670680.CrossRefGoogle Scholar
Laughlin, DC (2023) Plant strategies: the demographic consequences of functional traits in changing environments. Oxford University Press.CrossRefGoogle Scholar
Lortie, CJ and Aarssen, LW (1996) The specialization hypothesis for phenotypic plasticity in plants. International Journal of Plant Sciences 157, 484487.CrossRefGoogle Scholar
Lu, D, Zhu, J, Zhang, G, Fang, S, Sun, Y, Zhu, C, … & Wang, GG (2023) A forest gap is not forever: Towards an objective standard to determine when a gap is considered closed in temperate forests. Agricultural and Forest Meteorology 340, 109598.CrossRefGoogle Scholar
Łukowski, A, Giertych, MJ, Zadworny, M, Mucha, J and Karolewski, P (2015) Preferential feeding and occupation of sunlit leaves favors defense response and development in the flea beetle, Altica brevicollis coryletorum–a pest of Corylus avellana . PloS One 10, e0126072.CrossRefGoogle ScholarPubMed
Lundgren, MR and Des Marais, DL (2020) Life history variation as a model for understanding trade-offs in plant–environment interactions. Current Biology 30, R180R189.CrossRefGoogle Scholar
Luo, G, Li, J, Guo, S, Li, Y and Jin, Z (2022) Photosynthesis, nitrogen allocation, non-structural carbohydrate allocation, and C:N:P stoichiometry of Ulmus elongata seedlings exposed to different light intensities. Life 12, 1310.CrossRefGoogle Scholar
Matsuo, T, Martínez-Ramos, M, Bongers, F, van der Sande, MT and Poorter, L (2021) Forest structure drives changes in light heterogeneity during tropical secondary forest succession. Journal of Ecology 109, 28712884.CrossRefGoogle ScholarPubMed
Piper, FI, Altmann, SH and Lusk, CH (2018) Global patterns of insect herbivory in gap and understory environments, and their implications for woody plant carbon storage. Oikos 127, 483496.CrossRefGoogle Scholar
Poorter, L, Amissah, L, Bongers, F, Hordijk, I, Kok, J, Laurance, SG, … & van der Sande, MT (2023) Successional theories. Biological Reviews 98, 20492077.CrossRefGoogle ScholarPubMed
Poorter, L and Bongers, F (2006) Leaf traits are good predictors of plant performance across 53 rain forest species. Ecology 87, 17331743.CrossRefGoogle ScholarPubMed
R Core Team. (2023) R: a language and environment for statistical computing. Viena: R Foundation for Statistical Computing.Google Scholar
Richards, LA and Windsor, DM (2007) Seasonal variation of arthropod abundance in gaps and the understory of a lowland moist forest in Panama. Journal of Tropical Ecology 23, 169176.CrossRefGoogle Scholar
Rozendaal, DMA, Hurtado, VH and Poorter, L (2006) Plasticity in leaf traits of 38 tropical tree species in response to light; relationships with light demand and adult stature. Functional Ecology 20, 207216.CrossRefGoogle Scholar
Ruiz-Guerra, B, García, A, Velázquez-Rosas, N, Angulo, D and Guevara, R (2021) Plant-functional traits drive insect herbivory in a tropical rainforest tree community. Perspectives in Plant Ecology, Evolution and Systematics 48, 125587.CrossRefGoogle Scholar
Ruiz-Guerra, B, Nieves-Silva, E and Guevara, R (2017) The role of leaf traits and bird-mediated insect predation on patterns of herbivory in a semiarid environment in central Mexico. Botanical Sciences 95, 189201.CrossRefGoogle Scholar
Scheepens, JF, Deng, Y and Bossdorf, O (2018) Phenotypic plasticity in response to temperature fluctuations is genetically variable, and relates to climatic variability of origin, in Arabidopsis thaliana . AoB PLANTS 10, ply043.CrossRefGoogle ScholarPubMed
Stiegel, S, Entling, MH and Mantilla-Contreras, J (2017) Reading the leaves’ palm: leaf traits and herbivory along the microclimatic gradient of forest layers. PloS One 12, e0169741.CrossRefGoogle ScholarPubMed
Tripathi, S, Bhadouria, R, Srivastava, P, Devi, RS, Chaturvedi, R and Raghubanshi, AS (2020) Effects of light availability on leaf attributes and seedling growth of four tree species in tropical dry forest. Ecological Processes 9, 116.CrossRefGoogle Scholar
Valladares, F (2003) Light heterogeneity and plants: from ecophysiology to species coexistence and biodiversity. Progress in botany: Genetics; Physiology; Systematics; Ecology, pp. 439–471.CrossRefGoogle Scholar
Valladares, F and Niinemets, Ü (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annual Review of Ecology, Evolution, and Systematics 39, 237257.CrossRefGoogle Scholar
Valladares, F, Wright, J, Lasso, SE, Kitajima, K and Pearcy, RW (2000) Plastic phenotypic responses to light of 16 congeneric shrubs from a Panamanian rainforest. Ecology 81, 19251936.CrossRefGoogle Scholar
Zanne, AE, Lopez-Gonzalez, G, Coomes, DA, Ilic, J, Jansen, S, Lewis, SL, Miller, RB, Swenson, NG, Wiemann, MC, Chave, J and Lopez-Gonzalez, G (2009) Global Wood Density Database https://datadryad.org/stash/dataset/doi:10.5061/dryad.234.CrossRefGoogle Scholar
Zhang, T, Yan, Q, Wang, GG and Zhu, J (2021) The effects of stump size and within-gap position on sprout non-structural carbohydrates concentrations and regeneration in gaps vary among species with different shade tolerances. Ecological Processes 10, 114.CrossRefGoogle Scholar
Zhu, J, Tremblay, T and Liang, Y (2012) Comparing SPAD and atLEAF values for chlorophyll assessment in crop species, Canadian Journal of Soil Science 92, 645648.CrossRefGoogle Scholar
Supplementary material: File

Cadena-Zamudio et al. supplementary material

Cadena-Zamudio et al. supplementary material
Download Cadena-Zamudio et al. supplementary material(File)
File 2.7 MB