Acknowledgements
We would like to thank the Coordination for Personal Improvement of Higher Education Personnel (CAPES) for granting a scholarship, the Laboratory of Plant Anatomy (LAVeg) of the Federal University of Pernambuco (UFPE) for providing the space and materials to carry out this work, Lisi Alvarenga for the translation and revision of the manuscript. We also thank the Advanced Microscopy and Imaging Laboratory of the Center for Prospecting and Management of Biodiversity - Federal University of Pernambuco (LAMI-UFPE) and Hianna Fagundes for providing the Scanning Electron Microscope and images and Lucas da Penha Xavier for the statistical analyses of the data.
Conflicts of Interest
The authors declare that there are no conflicts of interest.
References
Abbas, M. W., Raza, A. B. M., Arshad, M., Ullah, M. I., Majeed, M. Z., & Aqueel, M. A. (2022). Plant defense to herbivore: Role of leaf epicuticular wax composition of citrus cultivars in citrus leafminer, Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) larval density. International Journal of Pest Management , 1-7. https://doi.org/10.1080/09670874.2022.2121874
Adler, L. S., Karban, R., & Strauss, S. Y. (2001). Direct and indirect effects of alkaloids on plant fitness via herbivory and pollination.Ecology , 82(7), 2032-2044. https://doi.org/10.1890/0012-9658(2001)082\%5b2032:DAIEOA\%5d2.0.CO;2
Ahmad, H. M., Rahman, M. U., Ali, Q., & Awan, S. I. (2015). Plant cuticular waxes: A review on functions, composition, biosyntheses mechanism and transportation. Life Science Journal , 12(4s), 60-67.
Almeida, N. M., Bezerra, T. T., Oliveira, C. R. S., Novo, R. R., Siqueira-Filho, J. A., Oliveira, P. E., & Castro, C. C. (2015). Breeding systems of enantiostylous Cassiinae species (Fabaceae, Caesalpinioideae). Flora-Morphology, Distribution, Functional Ecology of Plants , 215, 9-15. https://doi.org/10.1016/j.flora.2015.06.003
Almeida, N. M., Castro, C. C., Lima Leite, A. V., Novo, R. R., & Machado, I. C. (2013). Enantiostyly in Chamaecrista ramosa (Fabaceae-Caesalpinioideae): Floral morphology, pollen transfer dynamics and breeding system. Plant Biology , 15(2), 369-375. https://doi.org/10.1111/j.1438-8677.2012.00651.x
Almeida, N. M., Cotarelli, V. M., Souza, D. P., Novo, R. R., Siqueira Filho, J. A., Oliveira, P. E., & Castro, C. C. (2015). Enantiostylous types of Cassiinae species (Fabaceae-Caesalpinioideae). Plant Biology , 17(3), 740-745. https://doi.org/10.1111/plb.12283
Amorim, T., Marazzi, B., Soares, A. A., Forni-Martins, E. R., Muniz, C. R., & Westerkamp, C. (2017). Ricochet pollination in Senna (Fabaceae): Petals deflect pollen jets and promote division of labour among flower structures. Plant Biology , 19(6), 951-962. https://doi.org/10.1111/plb.12607
Aronne, G., Giovanetti, M., & De Micco, V. (2012). Morphofunctional traits and pollination mechanisms of Coronilla emerus L. flowers (Fabaceae). The Scientific World Journal , 2012. https://doi.org/10.1100/2012/381575
Avila-Sakar, G., Simmers, S. M., & Stephenson, A. G. (2003). The interrelationships among leaf damage, anther development, and pollen production in Cucurbita pepo ssp. texana (Cucurbitaceae).International Journal of Plant Sciences , 164(3), 395-404. https://doi.org/10.1086/374196
Barthlott, W., Neinhuis, C., Cutler, D., Ditsch, F., Meusel, I., Theisen, I., & Wilhelmi, H. (1998). Classification and terminology of plant epicuticular waxes. Botanical Journal of the Linnean Society , 126(3), 237-260. https://doi.org/10.1111/j.1095-8339.1998.tb02529.x
Bailes, E. J., & Glover, B. J. (2018). Intraspecific variation in the petal epidermal cell morphology of Vicia faba L. (Fabaceae).Flora , 244, 29-36. https://doi.org/10.1016/j.flora.2018.06.005
Bertness, M. D., & Shumway, S. W. (1992). Consumer-driven pollen limitation of seed production in marsh grasses. American Journal of Botany, 79(3), 288-293. https://doi.org/10.1002/j.1537-2197.1992.tb14550.x
Bukatsch, F. (1972). Bemerkungen zur Doppelfärbung: Astrablau-Safranin. Mikrokosmos, 61, 255.
Caldwell, E., Read, J., & Sanson, G. D. (2016). Which leaf mechanical traits correlate with insect herbivory among feeding guilds?Annals of Botany , 117(2), 349-361. https://doi.org/10.1093/aob/mcv178
Carper, A. L., Adler, L. S., & Irwin, R. E. (2016). Effects of florivory on plant-pollinator interactions: Implications for male and female components of plant reproduction. American Journal of Botany , 103(6), 1061-1070. https://doi.org/10.3732/ajb.1600144
Cavallini-Speisser, Q., Morel, P., & Monniaux, M. (2021). Petal cellular identities. Frontiers in Plant Science , 12, 745507. https://doi.org/10.3389/fpls.2021.745507
Corrêa, P. G., Pimentel, R. M. D. M., Cortez, J. S. D. A., & Xavier, H. S. (2008). Herbivoria e anatomia foliar em plantas tropicais brasileiras. Ciência e Cultura , 60(3), 54-57.
Cotarelli, V. M., & Almeida, A. N. M. (2015). Florivoria em Senna macranthera var. pudibunda (Benth.) H.S. Irwin & Barneby (Caesalpinioideae-Fabaceae). Nat Line , 13, 45-49.
Cotarelli, V. M., & Vieira, A. O. S. (2009). Herbivoria floral emChamaecrista trachycarpa (Vog.) H.S. Irwin & Barneby, em uma área de campo natural (Telêmaco Borba, PR, Brasil). Semina: Ciências Biológicas e da Saúde , 30(1), 91-98. https://doi.org/10.5433/1679-0367.2009v30n1p91
Costa, V. B. S., Pimentel, R. M. M., Chagas, M. G. S., Alves, G. D., & Castro, C. C. (2017). Petal micromorphology and its relationship to pollination. Plant Biology , 19(2), 115-122. https://doi.org/10.1111/plb.12523
Dai, H., Wang, Y., Du, Y., & Ding, J. (2010). Effects of plant trichomes on herbivores and predators on soybeans. Insect Science , 17(5), 406-413. https://doi.org/10.1111/j.1744-7917.2009.01305.x
David, R., & Carde, J. P. (1964). Coloration différentialle des pseodophylles de Pin maritime au moyen de reactif de Nadi. C. R. Acad. Sci. Paris, 258, 1338-1340.
Demis, E. (2024). Mechanism of plant resistance to insects, weeds and pathogens. Middle East Research Journal of Agriculture and Food Science , 4(2), 76-85. https://doi.org/10.36348/merjafs.2024.v04i02.005
Dulberger, R. (1981). The floral biology of Cassia didymobotrya and C. auriculata (Caesalpiniaceae). American Journal of Botany , 68(10), 1350-1360.
Erb, M., Züst, T., & Robert, C. A. M. (2021). Using plant chemistry to improve interactions between plants, herbivores and their natural enemies: Challenges and opportunities. Current Opinion in Biotechnology , 70, 262-265. https://doi.org/10.1016/j.copbio.2021.05.011
Furr, M., & Mahlberg, P. G. (1981). Histochemical analyses of laticifers and glandular trichomes in Cannabis sativa. Journal of Natural Products , 44(2), 153-159. https://doi.org/10.1021/np50014a002
Gorb, E. V., & Gorb, S. N. (2003). Capacidade de fixação do besouro Chrysolina fastuosa em várias superfícies de plantas. Entomologia Experimentalis et Applicata, 105(1), 13-28. https://doi.org/10.1046/j.1570-7458.2002.01028.x
Hanley, M. E., Lamont, B. B., Fairbanks, M. M., & Rafferty, C. M. (2007). Plant structural traits and their role in anti-herbivore defence. Perspectives in Plant Ecology, Evolution and Systematics , 8(4), 157-178. https://doi.org/10.1016/j.ppees.2007.01.001
Haas, S. M., & Lortie, C. J. (2020). A systematic review of the direct and indirect effects of herbivory on plant reproduction mediated by pollination. PeerJ , 8, e9049. https://doi.org/10.7717/peerj.9049
Jensen, W. A. (1962). Botanical histochemistry: principles and practice. W.H. Freeman and Company: San Francisco.
Johansen, D. A. (1940). Plant Microtechnique. McGraw Hill Book: New York.
Kariyat, R. R., Raya, C. E., Chavana, J., Cantu, J., Guzman, G., & Sasidharan, L. (2019). Feeding on glandular and non-glandular leaf trichomes negatively affect growth and development in tobacco hornworm (Manduca sexta) caterpillars. Arthropod-Plant Interactions , 13, 321-333. https://doi.org/10.1007/s11829-019-09678-z
Kaur, I., & Kariyat, R. (2023). Trichomes mediate plant–herbivore interactions in two Cucurbitaceae species through pre-and post-ingestive ways. Journal of Pest Science , 96(3), 1077-1089. https://doi.org/10.1007/s10340-023-01611-x
Kraaij, M., & van der Kooi, C. J. (2019). Surprising absence of association between flower surface microstructure and pollination system. Plant Biology , 22(2), 177-183. https://doi.org/10.1111/plb.13071
Kraus, J. E., & Arduin, M. (1997). Manual básico de métodos em morfologia vegetal. EDUR: Rio de Janeiro, Seropédica.
Kraus, J. E., et al. (1998). Astra blue and basic fuchsin double staining of plant materials. Biotechnic & Histochemistry , 73(5), 235-243.
Krupnick, G. A., & Weis, A. E. (1999). The effect of floral herbivory on male and female reproductive success in Isomeris arborea.Ecology , 80(1), 135-149. https://doi.org/10.1890/0012-9658(1999)080\%5b0135:TEOFHO\%5d2.0.CO;2
Kumar, S., Abedin, M. M., Singh, A. K., & Das, S. (2020). Role of phenolic compounds in plant-defensive mechanisms. In Plant phenolics in sustainable agriculture (pp. 517-532). https://doi.org/10.1007/97
Le Gall, M., & Behmer, S. T. (2014). Effects of protein and carbohydrate on an insect herbivore: the vista from a fitness landscape.Integrative and Comparative Biology . https://doi.org/10.1093/icb/icu102
Lewandowska, M., Keyl, A., & Feussner, I. (2020). Wax biosynthesis in response to danger: its regulation upon abiotic and biotic stress.New Phytologist , 227(3), 698-713. https://doi.org/10.1111/nph.16571
Lin, T., Doorduin, L., Temme, A., Pons, T. L., Lamers, G. E., Anten, N. P., & Vrieling, K. (2015). Enemies lost: parallel evolution in structural defense and tolerance to herbivory of invasive Jacobaea vulgaris. Biological Invasions , 17, 2339-2355. https://doi.org/10.1007/s10530-015-0879-2
Machado, R. A., Theepan, V., Robert, C. A., Züst, T., Hu, L., Su, Q., … & Erb, M. (2021). The plant metabolome guides fitness-relevant foraging decisions of a specialist herbivore. PLoS Biology , 19(2), e3001114. https://doi.org/10.1371/journal.pbio.3001114
Maêda, J. M. (1985). Manual para uso da câmara de Neubauer para contagem de pólen em espécies florestais. Universidade Federal do Rio de Janeiro, Rio de Janeiro.
Martini, F., Sun, I. F., & Chen, Y. Y. (2022). Effects of plant diversity and leaf traits on insect herbivory in plantation and natural forests. Forest Ecology and Management , 509, 120085. https://doi.org/10.1016/j.foreco.2022.120085
Mascarenhas, J. D. C., Beltrão, B. A., & Souza Junior, L. C. D. (2005). Projeto cadastro de fontes de abastecimento por água subterrânea no estado de Alagoas: diagnóstico do município de Quebrangulo. Recife: CPRM/PRODEEM.
Mason, C. J., Keefover‐Ring, K., Villari, C., Klutsch, J. G., Cook, S., Bonello, P., … & Townsend, P. A. (2019). Anatomical defences against bark beetles relate to degree of historical exposure between species and are allocated independently of chemical defences within trees.Plant, Cell & Environment , 42(2), 633-646. https://doi.org/10.1111/pce.13449
McCall, A. C. (2008). Florivory affects pollinator visitation and female fitness in Nemophila menziesii . Oecologia , 155(4), 729-737. https://doi.org/10.1007/s00442-007-0934-5
McCall, A. C., & Irwin, R. E. (2006). Florivory: the intersection of pollination and herbivory. Ecology Letters , 9(12), 1351-1365. https://doi.org/10.1111/j.1461-0248.2006.00975.x
Mithöfer, A., & Boland, W. (2012). Plant defense against herbivores: chemical aspects. Annual Review of Plant Biology , 63, 431-450. https://doi.org/10.1146/annurev-arplant-042110-103854
Mostafa, S., Wang, Y., Zeng, W., & Jin, B. (2022). Respostas de plantas à herbivoria, ferimentos e infecção. International Journal of Molecular Sciences , 23(13), 7031. https://doi.org/10.3390/ijms23137031
Nobrega, L. P., de Sá Haiad, B., & Ferreira, B. G. (2023). Epidermal and subepidermal changes during the formation of hairy galls induced by Eriophyidae on Avicennia schaueriana leaves. The Science of Nature , 110(5), 49. https://doi.org/10.1007/s00114-023-01876-3
Nusbaumer, L., Barbosa, M. R. V., Thomas, W. W., Alves, M. V., Loizeau, P. A., & Spichiger, R. (2015). Flora e vegetação da Reserva Biológica de Pedra Talhada. Boissiera, 68, 59-121.
Oguro, M., & Sakai, S. (2009). Floral herbivory at different stages of flower development changes reproduction in Iris gracilipes (Iridaceae).Plant Ecology , 202, 221-234. https://doi.org/10.1007/s11258-008-9461-7
Ojeda, I., Francisco-Ortega, J., & Cronk, Q. C. (2009). Evolution of petal epidermal micromorphology in Leguminosae and its use as a marker of petal identity. Annals of Botany , 104(6), 1099-1110. https://doi.org/10.1093/aob/mcp211
Paré, P. W., & Tumlinson, J. H. (1999). Plant volatiles as a defense against insect herbivores. Plant Physiology , 121(2), 325-332. https://doi.org/10.1104/pp.121.2.325
Patt, J. M., Merchant, M. W., Williams, E. R., & Meeuse, B. J. (1989). Pollination biology of Platanthera stricta (Orchidaceae) in Olympic National Park, Washington. American Journal of Botany , 76(8), 1097-1106. https://doi.org/10.1002/j.1537-2197.1989.tb15093.x
Pearse, A. G. E. (1985). Histochemistry: Theoretical and applied: Preparative and optical technology. (Churchill Livingston: Edinburgh).
Peeters, P. J. (2002). Correlations between leaf structural traits and the densities of herbivorous insect guilds. Biological Journal of the Linnean Society , 77(1), 43-65. https://doi.org/10.1046/j.1095-8312.2002.00091.x
Pritchard, D. J., & Vallejo-Marín, M. (2020). Buzz pollination.Current Biology , 30(15), R858-R860.
Quesada, M., Bollman, K., & Stephenson, A. G. (1995). Leaf damage decreases pollen production and hinders pollen performance inCucurbita texana. Ecology , 76(2), 437-443. https://doi.org/10.2307/1941202
Quiroz-Pacheco, E. N., Mora, F., Boege, K., Domínguez, C. A., & Del-Val, E. (2020). Effects of herbivory and its timing on reproductive success of a tropical deciduous tree. Annals of Botany , 126(5), 957-969. https://doi.org/10.1093/aob/mcaa117
R Core Team (2018). R: A language and environment for statiscal computing. R Foundation for. Statistical Computing, Vienna, Austria. URL https://www.R-Project.org/.
Rusman, Q., Poelman, E. H., Nowrin, F., Polder, G., & Lucas‐Barbosa, D. (2019). Floral plasticity: herbivore‐species‐specific‐induced changes in flower traits with contrasting effects on pollinator visitation.Plant, Cell & Environment , 42(6), 1882-1896. https://doi.org/10.1111/pce.13520
Souto, F. S., Lima e Silva, A., Santos, E. A. V., & Agra, M. D. F. (2022). Micromorphology of leaflets of Senna series Bacillares (Leguminosae) and its taxonomic significance. Botany , 100(12), 885-900. https://doi.org/10.1139/cjb-2022-0060
Van der Kooi, C. J., Elzenga, J. T. M., Dijksterhuis, J., & Stavenga, D. G. (2017). Functional optics of glossy buttercup flowers.Journal of the Royal Society Interface , 14(127), 20160933. https://doi.org/10.1098/rsif.2016.0933
Vázquez-González, C., Zas, R., Erbilgin, N., Ferrenberg, S., Rozas, V., & Sampedro, L. (2020). Resin ducts as resistance traits in conifers: linking dendrochronology and resin-based defences. Tree Physiology , 40(10), 1313-1326. https://doi.org/10.1093/treephys/tpaa064
Vidal, B. C. (1970). Dichroism in collagen bundles stained with xylidine-Ponceau 2R. Annales d’Histochimie , 15, 289-296.
Wari, D., Aboshi, T., Shinya, T., & Galis, I. (2022). Integrated view of plant metabolic defense with particular focus on chewing herbivores. Journal of Integrative Plant Biology , 64(2), 449-475. https://doi.org/10.1111/jipb.13204
Westerkamp, C. (2004). Ricochet pollination in Cassias–and how bees explain enantiostyly. Solitary Bees: Conservation, Rearing and Management for Pollination. Fortaleza: Universidade Federal do Ceará, 225-230.
Whitney, H. M., Kolle, M., Andrew, P., Chittka, L., Steiner, U., & Glover, B. J. (2009). Floral iridescence, produced by diffractive optics, acts as a cue for animal pollinators. Science , 323(5910), 130-133. https://doi.org/10.1126/science.1166256
Yadav, S. (2018). Lignin biosynthesis in plants and its role in anther dehiscence in Brassicaceae. The Botanica , 68, 48-59.