Abstract
Lophopterys floribunda is a Neotropical species of Malpighiaceae endemic to Brazil, occurring in both the Amazon and Atlantic Forest. Instead of the typical bi-glandular sepals reported for Neotropical Malpighiaceae, this species presents a single, large gland on the lateral sepals. In addition, ant patrolling was observed at the apex of bracts and bracteoles during fieldwork. Thus, this work aimed to describe the sepalar gland of L. floribunda and other secretory structures in its flowers and inflorescence. Samples of bracts, bracteoles, sepals, petals, and anther were collected and submitted to usual anatomical techniques. Unexpected nectaries at the apex of bracts and bracteoles, not visible to the naked eye, were described and represent a new type of structure for the family due to both their position and size. Mutualistic ants consume the exudate produced by these tiny nectaries, and such structures enable a specific visitation pattern for Lophopterys. Typical epithelial elaiophores occur on the lateral sepals, formed by an invaginated epidermis, which predominantly produce lipid secretion. The petal marginal glands are anatomically similar to the standard type of colleter, which exude mucilaginous substances. The exudate produced by the petal marginal glands was considered to have an additional role of contributing to the maintenance of the closed bud during the beginning of development. The globose epidermal cells containing lipids, proteins, and polysaccharides observed in the connective may be responsible for the typical aroma emitted by these flowers. The diversity of secretory structures reported here has application in both systematic and ecological studies of Malpighiaceae.
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Aliscioni SS, Gomiz NE, Agüero JI, Torretta JP (2022) Structural diversity of elaiophores in Argentine species of Malpighiaceae: morphology, anatomy, and interaction with pollinators. Protoplasma 259:789–807
Almeida RF, Francener A, Amorim AM (2016) A generic synopsis of Malpighiaceae in the Atlantic Forest. Nord J Bot 34:285–301. https://doi.org/10.1111/njb.01016
Almeida RF, Pessoa C, Francener A (2018) Sinopse de Malpighiaceae Juss. do Estado da Bahia, Brasil: chave para gêneros e monografias dos gêneros Alicia, Aspicarpa, Galphimia, Lophopterys, Mcvaughia e Verrucularia. Boletim Do Museu De Biologia Mello Leitão 40:55–91
Almeida RF, Guesdon IR, Pace MR, Meira RMSA (2019) Taxonomic revision of Mcvaughia WR Anderson (Malpighiaceae): notes on vegetative and reproductive anatomy and the description of a new species. PhytoKeys 117:45
Alves-Silva E, Bächtold A, Barônio GJ, Torezan-Silingardi HM, Del-Claro K (2014) Ant–herbivore interactions in an extrafloral nectaried plant: are ants good plant guards against curculionid beetles? J Nat Hist 49:841–851. https://doi.org/10.1080/00222933.2014.954020
Amorim M, De Marco P (2011) Pollination of Byrsonima coccolobifolia: short-distance isolation and possible causes for low fruit production. Braz J Biol 71:709–717. https://doi.org/10.1590/S1519-698420110004000166
Anderson WR (1979) Floral conservation in Neotropical Malpighiaceae. Biotropica 11:219–223
Anderson WR (1981) A botânica do altiplano de Guayana: parte 11. Malpighiaceae. Mem N Y Bot Gard 32:21–305
Anderson WR (1990) The origin of the Malpighiaceae - The evidence from morphology. Mem N Y Bot Gard 64:210–224
Anderson WR (2004) Malpighiaceae. In: Smith, N. & al. (ed.) Flowering Plants of the Neotropics 1:229–232
Anderson C, Anderson WR (2018) Revision of mezia (malpighiaceae). Edinb J Bot 75(3):321–376. https://doi.org/10.1017/S096042861800015X
Anderson WR, Davis CC (2001) Monograph of Lophopterys (Malpighiaceae). Contributions University Michigan Herbarium 23:83–105
Araújo JS (2014) Anatomia de espécies de Banisteriopsis c. B. Rob. (Malpighiaceae) ocorrentes no Brasil. 2014. 73f. Tese (Doutorado em Botânica) - Universidade Federal de Viçosa, Viçosa, MG
Araújo JS, Meira RMSA (2016) Comparative anatomy of calyx and foliar glands of Banisteriopsis CB Rob. (Malpighiaceae). Acta Botanica Brasilica 30:112–123. https://doi.org/10.1590/0102-33062015abb0248
Araújo JS, Azevedo AA, Silva LC, Meira RMSA (2010) Leaf anatomy as an additional taxonomy tool for 16 species of Malpighiaceae found in the Cerrado area (Brazil). Plant Syst Evol 286:117–131. https://doi.org/10.1007/s00606-010-0268-3
Arévalo-Rodrigues G, de Almeida RF, Cardoso-Gustavson P (2020) Anatomy of staminal glands in the Stigmaphylloid clade sheds light into new morphotypes of elaiophores and osmophores in Malpighiaceae. Plant Syst Evol 306:1–9. https://doi.org/10.1007/s00606-020-01680-w
Avalos AA, Pablo TJ, Lattar EC, Ferrucci MS (2020) Structure and development of anthers and connective glands in two species of Stigmaphyllon (Malpighiaceae): are heteromorphic anthers related to division of labour? Protoplasma 257:1165–1181
Avalos AA, Marrero HJ, Ferrucci MS, Torretta JP (2021) Stigmas arrangement, reproductive system, and maternal reproductive success in two species of Stigmaphyllon (Malpighiaceae): does pollinator size matter? Plant Ecol 222:1263–1279
Baker-Méio B, Marquis RJ (2012) Context-dependent benefits from ant–plant mutualism in three sympatric varieties of Chamaecrista desvauxii. J Ecol 100:242–252. https://doi.org/10.1111/j.1365-2745.2011.01892.x
Barônio GJ, Torezan-Silingardi HM (2017) Temporal niche overlap and distinct bee ability to collect floral resources on three species of Brazilian Malpighiaceae. Apidologie 48:168–180. https://doi.org/10.1007/s13592-016-0462-6
Barônio GJ, Haleem MA, Marsaioli AJ, Torezan-Silingardi HM (2017) Characterization of Malpighiaceae flower-visitor interactions in a Brazilian savannah: How do floral resources and visitor abundance change over time. Flora 234:126–134. https://doi.org/10.1016/j.flora.2017.07.015
BFG—Brazilian Flora Group (2015) Growing knowledge: an overview of Seed Plant diversity in Brazil. Rodriguésia 66:1085–1113
Caspary R (1848) De Nectariis. PhD Thesis. Elverfeldae, Bonn
Castro MA, Vega AS, Mulgura ME (2001) Structure and ultrastructure of leaf and calyx glands in Galphimia brasiliensis (Malpighiaceae). Am J Bot 88:1935–1944. https://doi.org/10.2307/3558420
Clark SG (1981) Staining procedures Williams & Wilkins. Baltimore
Cocucci AA, Holgado AM, Anton AM (1996) Estudio morfologico y anatomico de los eleoforos pedicelados de Dinemandra ericoides, Malpighiacea endemica del desierto de Atacama, Chile. Darwiniana 34:183–192
David R, Carde JP (1964) Coloration differentialle dês pseudophylles de Pin maritime au moyen reactif de Nadi. Comptes Rendus Hebdomadaires Des Seances De L Academie Des Sciences 258:1338–1340
Davis CC, Anderson WR (2010) A complete generic phylogeny of Malpighiaceae inferred from nucleotide sequence data and morphology. Am J Bot 97(12):2031–2048. https://doi.org/10.3732/ajb.1000146
Davis CC, Bell CD, Mathews S, Donoghue MJ (2002) Laurasian migration explains Gondwanan disjunctions: evidence from Malpighiaceae. Proc Natl Acad Sci 99(10):6833–7683. https://doi.org/10.1073/pnas.102175899
Davis CC, Schaefer H, Xi Z, Baum DA, Donoghue MJ, Harmon LJ (2014) Long-term morphological stasis maintained by a plant-pollinator mutualism. Proc Natl Acad Sci 111:5914–5919. https://doi.org/10.1073/pnas.1403157111
De Melo MC, Borba EL, Paiva EAS (2010) Morphological and histological characterization of the osmophores and nectaries of four species of Acianthera (Orchidaceae: Pleurothallidinae). Plant Syst Evol 286:141–151. https://doi.org/10.1007/s00606-010-0294-1
Del-Claro K (2010) Ant visitation to extrafloral nectaries decreases herbivory and increases fruit set in Chamaecrista debilis (Fabaceae) in a neotropical savanna. Flora 205:754–756. https://doi.org/10.1016/j.flora.2009.12.040
Del-Claro K, Marquis RJ (2015) Ant Species Identity has a Greater Effect than Fire on the Outcome of an Ant Protection System in Brazilian Cerrado. Biotropica 47:459–467. https://doi.org/10.1111/btp.12227
Delpino F (1868) Ulteriori osservazioni e considerazioni sulla dicogamia nel regno vegetale. Atti Della Societa Italiana Di Scienze Naturali e Dei Museo Civico Di Storia Et Naturale Di Milano 11:265–332
Elias TS, Gelband H (1976) Morphology and anatomy of floral and extrafloral nectaries in Campsis (Bignoniaceae). Am J Bot 63:1349–1353
Fahn A (1979) Secretory Tissues in Plants. Academic Press, London
Fahn A (1988) Secretory tissues in vascular plants. New Phytol 108:229–257
Feio AC, Ricarda R, Renata MSAM (2016) Secretory structures in leaves and flowers of two Dragon’s blood Croton (Euphorbiaceae): new evidence and interpretations. Int J Plant Sci 177:511–522. https://doi.org/10.1086/685705
Fernandes, G. Wilson, Fagundes, Marcílio, Greco, Magda K. Barcelos, Barbeitos, Marcos Soares e Santos, Jean Carlos (2005) Ants and their effects on an insect herbivore community associated with the inflorescences of Byrsonima crassifolia (Linnaeus) H.B.K. (Malpighiaceae). Revista Brasileira de Entomologia 49:264-269. https://doi.org/10.1590/S0085-56262005000200011
Fisher DB (1968) Protein staining of ribboned epon sections for light microscopy. Histochemie 16:92–96. https://doi.org/10.1007/BF00306214
Foster AS (1950) Practical plant anatomy. D. Van Nostrand Company Inc, Toronto
Gagliardi KB, Cordeiro I, Demarco D (2016) Protection and attraction: bracts and secretory structures in reduced inflorescences of Malpighiales. Flora - Morphol Distrib Funct Ecol Plants 220:52–62. https://doi.org/10.1016/j.flora.2016.02.003
Gates B (1982) Banisteriopsis and Diplopterys (Malpighiaceae). Flora Neotropica Monograph 30:1–237
Gonçalves-Souza P, Schlindwein C, Dötterl S, Paiva EAS (2017) Unveiling the osmophores of Philodendron adamantinum (Araceae) as a means to understanding interactions with pollinators. Ann Bot 119:533–543. https://doi.org/10.1093/aob/mcw236
Guesdon I (2017) Estruturas secretoras em linhagens Neo e Paleotropicais de Malpighiaceae: morfoanatomia, evidências funcionais e contribuições taxonômicas e evolutivas. 2017. 144f. Tese (Doutorado em Botânica) - Universidade Federal de Viçosa, Viçosa, MG
Guesdon IR, Amorim AM, Meira RMSA (2018) The hydrochorous Amazonian genus Glandonia (Malpighiaceae): new records, morphoanatomy updates and taxonomic contributions. Phytotaxa 345:13–25. https://doi.org/10.11646/phytotaxa.345.1.2
Guesdon IR, Amorim AM, Meira RMSA (2019) Functional role and evolutionary contributions of floral gland morphoanatomy in the Paleotropical genus Acridocarpus (Malpighiaceae). PLoS One 14:9. https://doi.org/10.1371/journal.pone.0222561
Johansen DA (1940) Plant microtechnique. McGraw Hill, New York
Kettler BA, Solís SM, Ferrucci MS (2018) Comparative survey of secretory structures and floral anatomy of Cohniella cepula and Cohniella jonesiana (Orchidaceae: Oncidiinae). New evidences of nectaries and osmophores in the genus. Protoplasma 255:1–18. https://doi.org/10.1007/s00709-018-1330-1
Kowalkowska AK, Pawłowicz M, Guzanek P, Krawczyńska AT (2018) Studies on floral nectary, tepals’ structure, and gynostemium morphology of Epipactis palustris (L.) Crantz (Orchidaceae) (L.) Crantz (Orchidaceae). Protoplasma 255:1811–1825. https://doi.org/10.1007/s00709-018-1274-5
Lersten NR, Horner HT Jr (1967) Development and structure of bacterial leaf nodules in Psychotria bacteriofila Val. (Rubiaceae). J Bacteriol 94:2027–2036
Machado SR, Morellato LPC, Sajo MG, Oliveira PS (2008) Morphological patterns of extrafloral nectaries in woody plant species of the Brazilian cerrado. Plant Biol 10:660–673. https://doi.org/10.1111/j.1438-8677.2008.00068.x
Matos RRD, Araújo JS (2021) Morfoanatomia das glândulas foliares e calicinais de Stigmaphyllon A. Juss. (Malpighiaceae): evidências funcionais, contribuições taxonômicas e evolutivas. Hoehnea 48:e282021. https://doi.org/10.1590/2236-8906-28/2021
Mayer JLS, Carmello-Guerreiro SM, Mazzafera P (2013) A functional role for the colleters of coffee flowers. Plantas AoB 5. https://doi.org/10.1093/aobpla/plt029
McManus JFA (1948) Histological and histochemical uses of periodic acid. Stain Technol 23:99–108. https://doi.org/10.3109/10520294809106232
Mello MAR, Bezerra ELS, Machado IC (2013) Functional roles of Centridini oil bees and Malpighiaceae oil flowers in biome-wide pollination networks. Biotropica 45:45–53. https://doi.org/10.1093/aobpla/plt029
Nery LA, Vieira MF, Ventrella MC (2017) Leaf glands of Banisteriopsis muricata (Malpighiaceae): distribution, secretion composition, anatomy and relationship to visitors. Acta Botanica Brasilica 31:459–467. https://doi.org/10.1590/0102-33062017abb0108
O’Brien TP, Feder N, Mccully ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59:368–373
Pacini E, Nepi M, Jl V (2003) Nectar biodiversity: a short review. Plant Syst Evol 238:7–22
Paiva EAS (2009) Occurrence, structure and functional aspects of the colleters of Copaifera langsdorffii Desf. (Fabaceae, Caesalpinioideae). CR Biol 332:1078–1084. https://doi.org/10.1016/j.crvi.2009.08.0033
Pansarin LM, Castro MM, Sazima M (2009) Osmophore and elaiophores of Grobya amherstiae (Catasetinae, Orchidaceae) and their relation to pollination. Bot J Linn Soc 159:408–415. https://doi.org/10.1111/j.1095-8339.2009.00953.x
Pansarin LM, Pansarin ER, Sazima M (2014) Osmophore structure and phylogeny of Cirrhaea (Orchidaceae, Stanhopeinae). Bot J Linn Soc 176:369–383. https://doi.org/10.1111/boj.12206
Pearse AGE (1980) Histochemistry: theoretical and applied, vol. 2, 4th edn. Churchill Livingstone, Edinburgh
Płachno BJ, Swiaztek P, Szymczak G (2010) Can astench be beautiful? Osmophores in stem-succu-lent stapeliads (Apocynaceae–Asclepiadoideae–Cero-pegieae–Stapeliinae). Flora 205:101–105. https://doi.org/10.1016/j.flora.2009.01.002
Possobom CCF, Machado SR (2017) Elaiophores: their taxonomic distribution, morphology and functions. Acta Botanica Brasilica 31:503–524. https://doi.org/10.1590/0102-33062017abb0088
Possobom CCF, Machado SR (2018) Elaiophores in three Neotropical Malpighiaceae species: a comparative study. Plant Syst Evol 304:15–32. https://doi.org/10.1007/s00606-017-1443-6
Possobom CCF, Guimarães E, Machado SR (2010) Leaf glands act as nectaries in Diplopterys pubipetala (Malpighiaceae). Plant Biol 12:863–870. https://doi.org/10.1111/j.1438-8677.2009.00304.x
Possobom CCF, Guimarães E, Machado SR (2015) Structure and secretion mechanisms of floral glands in Diplopterys pubipetala (Malpighiaceae), a neotropical species. Flora: Morphology. Distrib Funct Ecol Plants 211:26–39. https://doi.org/10.1016/j.flora.2015.01.002
Purvis MJ, Collier DC, Walls D (1964) Laboratory Techniques in Botany. Butterwoths, London
Ren MX, Zhong YF, Song XQ (2013) Mirror-image flowers without buzz pollination in the Asian endemic Hiptage benghalensis (Malpighiaceae). Bot J Linn Soc 173:764–774
Renner SS, Schaefer H (2010) The evolution and loss of oil-offering flowers: new insights from dated phylogenies for angiosperms and bees. Philos Trans Royal Soc b: Biol Sci 365:423–435. https://doi.org/10.1098/rstb.2009.0229
Rosumek FB, Silveira FA, Neves FDS, Barbosa NPDU, Diniz L, Oki Y, Cornelissen T (2009) Ants on plants: a meta-analysis of the role of ants as plant biotic defenses. Oecologia 160:537–549. https://doi.org/10.1007/s00442-009-1309-x
Sazima M, Vogel S, Cocucci A, Hausner G (1993) The perfume flowers of Cyphomandra (Solanaceae): Pollination by euglossine bees, bellows mechanism, osmophores, and volatiles. Plant Syst Evol 187:51–88
Schmid R (1988) Reproductive versus extra-reproductive nectaries—historical perspective and terminological recommendations. Bot Rev 54:179–227
Simpson BB, Neff JL (1981) Floral rewards: alternatives to pollen and nectar. Ann Mo Bot Gard 68:301–322
Subramanian RB, Arumugasamy K, Inamdar JS (1990) Studies in secretory glands of Hiptage sericea (Malpighiaceae). Nord J Bot 10:57–62. https://doi.org/10.1111/j.1756-1051.1990.tb01753.x
Teixeira LAG, Machado IC (2000) Sistema de polinização e reprodução de Byrsonima sericea DC (Malpighiaceae). Acta Botanica Brasilica 14:347–357
Thomas V (1991) Structural, functional and phylogenetic aspects of the colleter. Ann Bot 68:287–305. https://doi.org/10.1093/oxfordjournals.aob.a088256
Tölke ED, Bachelier JB, de Lima EA, Ferreira MJP, Demarco D, Carmello-Guerreiro SM (2018) Osmophores and floral fragrance in Anacardium humile and Mangifera indica (Anacardiaceae): an overlooked secretory structure in Sapindales. Plantas AoB 10:1–14. https://doi.org/10.1093/aobpla/ply062
Vogel S (1990) History of the Malpighiaceae in the Light of Pollination Ecology. Mem N Y Bot Gard 55:130–142
Wiemer AP, More M, Benitez-Vieyra S, Cocucci AA, Raguso RA, Sersic AN (2009) A simple floral fragrance and unusual osmophore structure in Cyclopogon elatus (Orchidaceae). Plant Biol 11:506–514. https://doi.org/10.1111/j.1438-8677.2008.00140.x
Acknowledgements
This work was carried out with support from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Financing Code 001. We thank the funding agencies FAPEMIG (Fundação de Amparo à Pesquisa do Estado de Minas Gerais) and Proap (Programa de Apoio à Pós-graduação) for supporting collection and field work. Renata Meira (DEB #307987/2022-1) thanks CNPq for her productivity grants. We also thank Roberto Paulino Pereira, the guide of the RPPN, for accompaniment in the field and Júlio Cézar Mário Chaul for the identification of the collected insects.
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Sanches, M.M., Guesdon, I.R. & Alves Meira, R.M.S. Diversity and functional roles of floral glands in Malpighiaceae: insights in Lophopterys floribunda W.R. Anderson & C. Davis. Protoplasma 260, 1555–1567 (2023). https://doi.org/10.1007/s00709-023-01871-5
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DOI: https://doi.org/10.1007/s00709-023-01871-5