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.