Abstract
The flowers of the species of Malpighiaceae in the Neotropical Region are relatively uniform in their morphology due to their dependence on oil-collecting bees as their main pollinators. However, many species of the genus Galphimia seem to have acquired a different floral syndrome, lacking markedly zygomorphic flowers and developed elaiophores in the calyx. Likewise, these species present anthers with great development, probably in response to the selection of pollinators that collect pollen. Galphimia australis incorporated some of these traits but also retained some residual characteristics typical of species pollinated by oil bees. This leads to many questions on how these flowers ensure their pollination. Inquiring about the reduction or modification of these characteristics allows us to understand how G. australis achieves a different pollination syndrome. In this research, we carry out a detailed morphological and anatomical study of the flowers and pollen grain devolvement of G. australis and floral visitors were observed and captured. Results were analyzed in order to determine how this species changed from the oil-floral syndrome, typical of neotropical Malpighiaceae, to one syndrome with pollen as the main reward.
Similar content being viewed by others
Data availability
Data sharing not applicable to this article as no datasets were generated or analysed during the current study.
References
Adachi SA, Machado SR (2020) Lip morphology and ultrastructure of osmophores in Cyclopogon (Orchidaceae) reveal a degree of morphological differentiation among species. Protoplasma 257:1139–1148. https://doi.org/10.1007/s00709-020-01499-9
Aliscioni S, 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. https://doi.org/10.1007/s00709-021-01699-x
Aliscioni SS, Gotelli M, Torretta JP (2018) Structure of the stigma and style of Callaeum psilophyllum (Malpighiaceae) and its relation with potential pollinators. Protoplasma 255:1433–1442. https://doi.org/10.1007/s00709-018-1245-x
Aliscioni SS, Gotelli M, Torretta JP (2019) Gynoecium with carpel dimorphism in Tricomaria usillo, comparison with other genera of the Carolus clade (Malpighiaceae). Protoplasma 256:1133–1144. https://doi.org/10.1007/s00709-019-01373-3
Aliscioni SS, Torretta JP (2017) Malpighiaceae. In: Zuloaga FO, Belgrano MJ (eds) Flora Vascular de la República Argentina, 17. Estudio Sigma S.R.L., Buenos Aires, pp 163–205
Anderson CE (2005) Galphimia (Malpighiaceae) in South America. Contrib Univ Michigan Herb 24:1–12
Anderson CE (2007) Revision of Galphimia (Malpighiaceae). Contr Univ Michigan Herb 25:1–82
Anderson WR (1977) Byrsonimoideae, a new subfamily of the Malpighiaceae. Leandra 7:5–18
Anderson WR (1979) Floral conservatism in neotropical Malpighiaceae. Biotropica 11:219–222. https://doi.org/10.2307/2388042
Anderson WR (1990) The origin of the Malpighiaceae. The evidence from morphology. Mem New York Bot Gard 64:210–222
Anderson WR, Anderson C, Davis CC (2006) Malpighiaceae. http://herbarium.lsa.umich.edu/malpigh/index.html [accessed on 11.11.2022]
Araújo JS, Meira RMSA (2016) Comparative anatomy of calyx and foliar glands of Banisteriopsis CB Rob. (Malpighiaceae). Acta Bot Brasil 30:112–123. https://doi.org/10.1590/0102-33062015abb0248
Ashworth L, Aguilar R, Martén-Rodríguez S, Lopezaraiza-Mikel M, Avila-Sakar G, Rosas-Guerrero V, Quesada M (2015) Pollination syndromes: a global pattern of convergent evolution driven by the most effective pollinator. In: Pontarotti P, ed. Evolutionary biology. Biodiversification from genotype to phenotype. Cham, Switzerland, pp 203–224
Avalos AA, Torretta JP, 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. https://doi.org/10.1007/s00709-020-01497-x
Cameron KM, Chase MW, Anderson WR, Hills HG (2001) Molecular systematics of Malpighiaceae: evidence from plastid rbcL and matK sequences. Amer J Bot 88:1847–1918. https://doi.org/10.2307/3558361
Cappellari SC, Haleem MA, Marsaioli AJ, Tidon R, Simpson BB (2011) Pterandra pyroidea: a case of pollination shift within Neotropical Malpighiaceae. Ann Bot 107:1323–1334. https://doi.org/10.1093/aob/mcr084
Castro MDM, Demarco D (2008) Phenolic compounds produced by secretory structures in plants: a brief review. Nat Prod Commun 3:1273–1284
Castro MA, Vega AS, Múlgura ME (2001) Structure and ultrastructure of leaf and calyx glands in Galphimia brasiliensis (Malpighiaceae). Amer J Bot 88:1935–1944
Cocucci AA, Holgado AM, Anton AM (1996) Estudio morfológico y anatómico de los eleóforos pedicelados de Dinemandra ericoides, Malpigiácea endémica del desierto de Atacama, Chile. Darwiniana 34:183–192. https://doi.org/10.14522/darwiniana.2014.341-4.404
Curry KJ, McDowell LM, Judd WS, Stern WL (1991) Osmophores, floral features, and systematics of Stanhopea (Orchidaceae). Amer J Bot 78:610–623. https://doi.org/10.1002/j.1537-2197.1991.tb12585
Dalmazzo M, González-Vaquero RA, Roig-Alsina A, Debandi G (2014) Halictidae. In: Roig-Juñent S, Claps LE, Morrone JJ. Biodiversidad de Artrópodos Argentinos IV. Ed. INSUE, Universidad Nacional de Tucumán, San Miguel de Tucumán, Argentina, pp. 203–219.
David R, Carde JP (1964) Coloration differential le des inclusions lipidiques terpeniques des pseudo phylles du pin maritime au moyen du react if Nadi. Comptes Rendus 258:1338–1340
Davis G (1966) Systematic embryology of the angiosperms. Wiley, New York
Davis CC, Anderson WR (2010) A complete generic phylogeny of Malpighiaceae inferred from nucleotide sequence data and morphology. Amer J Bot 97:2031–2048. https://doi.org/10.3732/ajb.1000146
Davis CC, Anderson WR, Donoghue MJ (2001) Phylogeny of Malpighiaceae: evidence from chloroplast ndhF and trnl-F nucleotide sequences. Amer J Bot 88:1830–1846. https://doi.org/10.2307/3558360
Davis CC, Schaefer H, Xi Z, Baum DA, Donoghue MJ, Harmon LJ (2014) Long-term morphological stasis maintained by a plant-pollinator mutualism. PNAS 111:5914–5919. https://doi.org/10.1073/pnas.1403157111
Davis CC, Marinho LC, Amorím AA (2020) Andersoniella: a new genus of Neotropical Malpighiaceae. Harvard Pap Bot 25:51–56. https://doi.org/10.3100/hpib.v25iss1.2020.n6
Dellinger AS (2020) Pollination syndromes in the 21st century: where do we stand and where may we go? New Phytol 228:1193–1213
Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Ann Rev Ecol Evol Syst 35:375–403
Evert RF (2006) Esau’s plant anatomy: meristems, cells, and tissues of the plant body: their structure, function, and development. John Wiley & Sons. https://doi.org/10.1002/0470047380
Gaglianone MC (2003) Abelhas da tribo Centridini na Estação Ecológica de Jataí (Luis Antônio, SP): composição de espécies e interações com flores de Malpighiaceae. In: Melo GAR, Alves-dos Santos I (eds.). Apoidea Neotropica: Homenagem aos 90 anos de Jesus Santiago Moure. Editora UNESC, Criciúma, pp. 279–284
Galati BG (2003) Ubisch bodies in angiosperms. Advances Pl Reprod Biol 2:1–20
Galati BG, Gotelli MM, Dolinko AE, Rosenfeldt S (2019) Could microechinate orbicules be related to the release of pollen in anemophilous and ‘buzz pollination’species? Aust J Bot 67:16–35. https://doi.org/10.1071/BT18169
Gates B (1982) Banisteriopsis, Diplopterys (Malpighiaceae). Flora Neotropica 30:1–237
Hassanpour S, Maherisis N, Eshratkhah B (2011) Plants and secondary metabolites (Tannins): r review. Int J Forest Soil Erosion 1:47–53
Huysmans S, El-Ghazaly G, Smets E (1998) Orbicules in angiosperms: morphology, function, distribution, and relation with tapetum types. Bot Rev 64:240–272. https://doi.org/10.1007/BF02856566
Jensen W (1962) Botanical histochemistry. Freeman, San Francisco
Johansen DA (1940) Plant microtechnique. McGraw-Hill Book Company Inc, London
Johri BM, Ambegaokar KB, Srivastava PS (1992) Comparative embriology of angiosperms, vol 1. Springer-Verlag, Berlin
Kowalkowska AK, Kozieradzka-Kiszkurno M, Turzyński S (2015) Morphological, histological and ultrastructural features of osmophores and nectary of Bulbophyllum wendlandianum (Kraenzl.) Dammer (B. section Cirrhopetalum Lindl., Bulbophyllinae Schltr., Orchidaceae). Plant Syst Evol 301:609–622. https://doi.org/10.1007/s00606-014-1100-2
Lobreau-Callen D (1983) Analyse de la repartition géographique des Malphigiaceae d’apres les caractêres du pollen et de la pollinisation. Bothalia 14:871–881
Lobreau-Callen D (1984) Pollens and apoids of Senegal: pollination and behaviour. Rev Paléobiol 131–138.
Lobreau-Callen D (1989) Les Malpighiaceae et leurs pollinisateurs. Coadaptation Ou Coevolution Adansonia 11:79–94
Lowrie SR (1982) The Palynology of the Malpighiaceae and its contribution to family systematics. PhD Dissertation, University of Michigan
Marinho CR, Souza CD, Barros TC, Teixeira SDP (2014) Scent glands in legume flowers. Plant Biol 16:215–226. https://doi.org/10.1111/plb.12000
Miyashita RK, Nakasone HY, Lamoureux CH (1964) Reproductive morphology of acerola (Malpighia glabra L.). Hawaii Agricultural Experiment Station, University of Hawaii.
Neff JL, Simpson BB (1981) Oil-collecting structures in the Anthophoridae (Hymenoptera): morphology, function, and use in systematics. J Kansas Entomol Soc 54:95–123
Pacek A, Stpiczynska M (2007) The structure of elaiophores in Oncidium cheirophorum Rchb. f. and Ornithocepha luskruegeri Rchb. f. [Orchidaceae]. Acta Agrobot 60:9–14
Pearse AGE, Hess R (1961) Substantivity and other factors responsible for formazan patterns in dehydrogenase histochemistry. Experientia 17:136–141. https://doi.org/10.1007/BF02160833
Possobom CCF, Guimarães E, Machado SR (2015) Structure and secretion mechanisms of floral glands in Diplopterys pubipetala (Malpighiaceae), a neotropical species. Flora 211:26–39
Possobom CCF, Machado SR, Guimarães E (2016) Reproductive system of Diplopterys pubipetala (Malpighiaceae) plants from a savanna ecosystem. Inter J Plant Repr Biol 8:7–13
Possobom CCF, Machado SR (2017) Elaiophores: their taxonomic distribution, morphology and functions. Acta Bot Brasil 31:503–524. https://doi.org/10.1590/0102-33062017abb0088
Possobom CC, 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
Qian Z, Meng Q, Ren M (2016) Pollination ecotypes and herkogamy variation of Hiptage benghalensis (Malpighiaceae) with mirror-image flowers. Biodiv Sci 24:1364–1372. https://doi.org/10.17520/biods.2016248
Roig-Alsina A (2013) El género Ceratina en la Argentina: revisión del subgénero Neoclaviceras ubg. n. (Hymenoptera, Apidae, Xylocopinae). Rev Mus Argentino Cienc Nat, ns15:121–143
Sazima M, Sazima I (1989) Oil-gathering bees visit flowers and glandular morphs of the oil-producing Malpighiaceae. Bot Acta 102:106–111. https://doi.org/10.1111/j.1438-8677.1989.tb00073.x
Simpson BB, Neff JL (1983) Evolution and diversity of floral rewards. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Van Nostrand Reinold Co, New York, pp 142–159
Siddiqui SA (1968) The microsporangium and the male gametophyte in Malpighia coccigera Linn. Beitr Biol Pflanzen 44:361–364
Singh B (1959) Studies in the family Malpighiaceae. 1. Morphology of Thryallis glauca Kuntze. Hortic Adv 3:1–19
Sigrist MR, Sazima M (2004) Pollination and reproductive biology of twelve species of neotropical Malpighiaceae: stigma morphology and its implications for the breeding system. Ann Bot 94:33–41
Sokoloff DD, Nuraliev MS, Oskolski AA, Remizowa MV (2017) Gynoecium evolution in angiosperms: monomery, pseudomonomery, and mixomery. Mosc Univer Biol Sci 72:97–108. https://doi.org/10.3103/S0096392517030105
Steiner KE (1985) Functional dioecism in the Malpighiaceae: the breeding system of Spachea membranacea Cuatr. Amer J Bot 72:1537–1543
Stern WL, Curry, KJ, Pridgeon AM (1987) Osmophores of Stanhopea (Orchidaceae). Amer J Bot 74.1323–1331. https://doi.org/10.1002/j.1537-2197.1987.tb08747.x
Subramanian RB, Arumugasamy K, Inamdar JA (1990) Studies in the secretory glands of Hiptage sericea (Malpighiaceae). Nord J Bot 10:57–62. https://doi.org/10.1111/j.1756-1051.1990.tb01753.x
Torretta JP, Aliscioni SS, González-Arzac A, Avalos AA (2017) Is the variation of floral elaiophore size in two species of Stigmaphyllon (Malpighiaceae) dependent on interaction with pollinators? Plant Ecol Divers 10:403–418
Torretta JP, Aliscioni SS, Marrero HJ, Avalos AA (2022) Oil flowers of Malpighiaceae and its oil-collecting bees: loyalty and robbery in a highly specialized system. Apidologie 53:1–15
Torretta JP, Roig-Alsina A (2017) Las abejas colectoras de aceite del género Paratetrapedia (Hymenoptera, Apidae, Tapinotaspidini) en la Argentina. Revista del Museo Argentino de Ciencias Naturales 19(2):131–140
von Ubisch G (1927) Zur Entwicklungsgeschichte der Antheren. Planta 3:490–495
Vogel S (1974) Ölblumen und ölsammelnde Bienen. Tropische Und Subtropische Pflanzenwelt 7:283–547
Vogel S (1990) History of the Malpighiaceae in the light of pollination ecology. Mem New York Bot Gard 55:130–142
Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060
Zarlavsky GE (2014) Histología Vegetal: técnicas simples y complejas. Sociedad Argentina de Botánica, Buenos Aires, Argentina.
Zhang W, Kramer EM, Davis CC (2016) Differential expression of CYC2 genes and the elaboration of floral morphologies in Hiptage, an Old World genus of Malpighiaceae. Int J Plant Sci 177:551–558. https://doi.org/10.1086/687225
Acknowledgements
We thank G. Zarvlasky for technical assistance; A. Roig-Alsina for helping with the determination of some bees; two anonymous reviewers for valuable comments, and the Administración de Parque Nacionales (Project NEA 294), and the Ministerio de Ecología y Recursos Naturales Renovables, province of Misiones, (Project “Estudio integral de interacciones entre especies de Malpighiaceae y sus polinizadores”), for permission to conduct part of this study in protected areas.
Funding
This work was funded by a research grant from Agencia Nacional de Promoción Científica y Tecnológica, grant number PICT 2013–1867 to S. Aliscioni, Consejo Nacional de Investigaciones Científicas y Técnicas, grant number PIP 11220110100312 to J.P. Torretta and Universidad de Buenos Aires, UBACyT 20020130200203BA and 20020170200252BA to J.P. Torretta. M. M. Gotelli, S. S. Aliscioni and J. P. Torretta are affiliated with Consejo Nacional de Investigaciones Científicas y Técnicas, and Universidad de Buenos Aires, Argentina.
This study was performed with permission of the Administración de Parque Nacionales (Regional NEA), and the Ministerio de Ecología y Recursos Naturales Renovables, province of Misiones.
Author information
Authors and Affiliations
Contributions
MG, SA and JPT contributed to the study conception and design. Data collection and analysis were performed by JPT. Morphological observations were made by PTK and SA. Flowers were processed for microscope observations and analyzed by SA, PTK and MG. The first draft of the manuscript was written by MG, SA and JPT; all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.
Conflict of interest
The authors declare no conflict of interest.
Additional information
Handling Editor: Dorota Kwiatkowska
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) 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
Gotelli, M., Aliscioni, S., Kuo, P.T. et al. Are the floral morphology and anatomy of Galphimia australis, an atypical neotropical Malpighiaceae, associated to a new pollination syndrome?. Protoplasma 260, 1047–1062 (2023). https://doi.org/10.1007/s00709-022-01829-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-022-01829-z