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Gynoecium with carpel dimorphism in Tricomaria usillo, comparison with other genera of the Carolus clade (Malpighiaceae)

  • Sandra Silvina AliscioniEmail author
  • Marina Gotelli
  • Juan Pablo Torretta
Original Article


We analyzed the gynoecium morphology and anatomy of Tricomaria usillo in young and mature flowers from diverse populations in order to analyze the differentiation of structure and function of the parts of the carpel. We also aimed to find the potential pollinators and associate the morphology of the gynoecium with its role. We compare the characteristics of the gynoecium of T. usillo and discuss the carpel dimorphism with other genera within the Carolus clade in relation with their pollination syndromes. Carpels were processed according to classic techniques for scanning electron microscopy and bright field microscopy. We conducted field observation in different populations of T. usillo and captured the insects that were identified to specific level. The gynoecium of T. usillo shows inter-population and intra-individual variability. Some have three well-developed carpels, while most of them present two posterior carpels with differentiated styles and stigmas and the anterior one with a shorter style with or without stigma. The ovary has three locules with one ovule each. A compitum is formed and all ovules may be fecundated. However, fruits have generally one seed that develops in the anterior locule. Centris brethesi is the potential pollinator. The gynoecium of T. usillo reflects part of the variation in the carpel dimorphism that probably arose in the branch of the Carolus clade, and evolved in diverse ways in the lineages of this group. Tricomaria usillo seems to represent a recent transition towards reaching a stable form of carpel dimorphism and definitive division of labors of the carpels.


Anatomy Compitum Pollination Style Stigma 



We thank G. Zarvlasky for technical assistance; A. Calviño for providing material from La Cantina, Córdoba; R. Saurral for the revision of the English language; and two anonymous reviewers.

Funding information

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, and Universidad de Buenos Aires, grant number UBACyT 20020130200203BA to J. P. Torretta. Sandra Aliscioni, Marina Gotelli and Juan Pablo Torretta are affiliated with Consejo Nacional de Investigaciones Científicas y Técnicas, and Universidad de Buenos Aires, Argentina.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical 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.


  1. Aliscioni SS, Torreta JP (2017) Malpighiaceae. Pages 163–205 in Flora Argentina, eds. Zuloaga FO, Belgrano MJ, Vol 17, Sigma, Buenos AiresGoogle Scholar
  2. Aliscioni SS, Gotelli M, Torretta JP (2018) Structure of the stigma and style of Callaeum psilophyllum (Malpighiaceae) and its relation with potential pollinators. Protoplasma 255:1433–1442CrossRefGoogle Scholar
  3. Anderson WR (1979) Floral conservatism in neotropical Malpighiaceae. Biotropica 11:219–223CrossRefGoogle Scholar
  4. Anderson WR (1990) The origin of the Malpighiaceae. The evidence from morphology. Mem New York Bot Gard 64:210–224Google Scholar
  5. Anderson WR (2006) Eight segregates from the neotropical genus Mascagnia (Malpighiaceae). Novon 16:168–204CrossRefGoogle Scholar
  6. Anderson WR, Anderson C, Davis CC (2006) Malpighiaceae. [January 2019]
  7. Armbruster WS, Debevec EM, Wilson MF (2002) Evolution of syncarpy in angiosperms: theoretical and phylogenetic analyses of the effects of carpel fusion on offspring quantity and quality. J Evol Biol 15:657–672CrossRefGoogle Scholar
  8. Arumuganathan K, Udaiyan K, Sugavanam V (1994) Structure and ontogeny of floral and extrafloral nectaries in Hiptage benghalensis (L.) Kurz (Malpighiaceae). Adv Plant Sci 7:105–111Google Scholar
  9. Arumugasamy K, Inamdar JA, Subramanian RB (1989) Structure, ontogeny and secretion of oil secreting glands in Hiptage acuminate Wall. Curr Sci 58:260–261Google Scholar
  10. Bailey IW, Swamy BGL (1951) The conduplicate carpel of dicotyledons and its initial trends of specialization. Am J Bot 38:373–379CrossRefGoogle Scholar
  11. Baum H (1948) Postgenitale Verwachsung in und zwischen Karpell- und Staubblattkreisen. Sitz ber Österr Akad Wiss Math-Natur-wiss Kl, Abt1 157:17–38Google Scholar
  12. Cameron KM, Chase MW, Anderson WR, Hills HG (2001) Molecular systematics of Malpighiaceae: evidence from plastid rbcL and matK sequences. Amer J Bot 88:1847–1862CrossRefGoogle Scholar
  13. Chase MW (1981) A revision of Dicella (Malpighiaceae). Syst Bot 6:159–171CrossRefGoogle Scholar
  14. Davis CC, Anderson WR (2010) A complete generic phylogeny of Malpighiaceae inferred from nucleotide sequence data and morphology. Amer J Bot 97:2031–2048CrossRefGoogle Scholar
  15. Davis CC, Anderson WR, Donoghue MJ (2001) Phylogeny of Malpighiaceae: evidence from chloroplast ndhF and trnl-F nucleotide sequences. Amer J Bot 88:1830–1846CrossRefGoogle Scholar
  16. Davis CC, Fritsch PW, Bell CD, Mathews S (2004) High-latitude tertiary migrations of an exclusively tropical clade: evidence from Malpighiaceae. Int J Pl Sci 165:S107–S121CrossRefGoogle Scholar
  17. Davis CC, Schaefer H, Xi Z, Baum DA, Donoghue MJ, Harmon LJ (2014) Long-term morphological stasis maintained by a plant-pollinator mutualism. Proc National Acad Sci USA 111:5914–5919CrossRefGoogle Scholar
  18. Doyle JA, Endress PK (2000) Morphological phylogenetic analysis of basal angiosperms: comparison and combination with molecular data. Int J Plant Sci 161:121–153CrossRefGoogle Scholar
  19. Endress PK (1982) Syncarpy and alternative modes of escaping disadvantages of apocarpy in primitive angiosperms. Taxon 31:48–52CrossRefGoogle Scholar
  20. Endress PK (2001) The flowers in extant basal angiosperms and inferences on ancestral flowers. Int J Plant Sci 162:1111–1140CrossRefGoogle Scholar
  21. Endress PK (2011) Evolutionary diversification of the flowers in angiosperms. Am J Bot 98:370–396CrossRefGoogle Scholar
  22. Endress PK (2015) Patterns of Angiospermy development before carpel sealing across living angiosperms: diversity, and morphological and systematic aspects. Bot J Linn Soc 178:556–591CrossRefGoogle Scholar
  23. Endress PK, Doyle JA (2009) Reconstructing the ancestral flower and its initial specializations. Am J Bot 96:22–66CrossRefGoogle Scholar
  24. Endress PK, Igersheim A (2000) Gynoecium structure and evolution in basal angiosperms. Int J Plant Sci 161:211–223CrossRefGoogle Scholar
  25. Launert E (1968) Malpighiaceae. Flora of tropical East Africa. 24 pp.Google Scholar
  26. Leme FM, Staedler YM, Schönenberger J, Teixeira SP (2018) Ontogeny and vascularization elucidate the atypical floral structure of Ampelocera glabra, a tropical species of Ulmaceae. Int J Plant Sci 179:461–476CrossRefGoogle Scholar
  27. Niedenzu FJ (1928) Malpighiaceae Pars I Pages 67–84 in Das Pflanzenreich, ed. A Engler. IV, 141Google Scholar
  28. Qian ZN, Meng QW, Ren MX (2016) Pollination ecotypes and herkogamy variation of Hiptage benghalensis (Malpighiaceae) with mirror-image flowers. Biodivers Sci 24:1364–1372CrossRefGoogle Scholar
  29. Roig Alsina A (2000) Claves para las especies argentinas de Centris (Hymenoptera, Apidae), con descripción de nuevas especies y notas sobre distribución. Revista Mus Argent Ci Nat, N S 2:171–193CrossRefGoogle Scholar
  30. Siegel BA, Verbeke JA (1989) Diffusible factors essential for epidermal cell redifferentiaion in Catharanthus roseus. Science 244:580–582CrossRefGoogle Scholar
  31. 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 94:33–41CrossRefGoogle Scholar
  32. Sokoloff DD, Nuraliev MS, Oskolski AA, Remizowa MV (2017) Gynoecium evolution in angiosperms: monomery, pseudomonomery, and mixomery. Mosc Univ Biol Sci Bull 72:97–108CrossRefGoogle Scholar
  33. Stebbins GL (1974) Flowering plants: evolution above the species level. Harvard University Press, CambridgeCrossRefGoogle Scholar
  34. Subramanian RB, Arumugasamy K, Inamdar JA (1990) Studies in the secretory glands of Hiptage sericea (Malpighiaceae). Nord J Bot 10:57–62CrossRefGoogle Scholar
  35. Thiers B (2014) Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. Available from: (accessed December 2018)
  36. Verbeke JA (1992) Fusion events during floral morphogenesis. Annual Rev Pl Biol 43:583–598CrossRefGoogle Scholar
  37. Vogel S (1990) History of the Malpighiaceae in the light of pollination ecology. Mem New York Bot Gard 55:130–142Google Scholar
  38. Walker DB (1975) Postgenital carpel fusion in Catharanthus roseus (Apocynaceae). I. Light and scanning electron microscopic study of gynoecial ontogeny. Am J Bot 62:457–467CrossRefGoogle Scholar
  39. Wilczek R (1955) Novitates africanae I (Malpighiaceae et Linaceae). Bull Jard Bot État Bruxelles 25:303–313CrossRefGoogle Scholar
  40. Wilczek R (1959) Novitates africanae VI Flabellariopsis acuminata (Engl.) R. Wilczek descr. ampl. Bull Jard Bot État Bruxelles 29:193–194CrossRefGoogle Scholar
  41. Zarlavsky GE (2014) Histología Vegetal: técnicas simples y complejas. Sociedad Argentina de Botánica, Buenos Aires, ArgentinaGoogle Scholar
  42. 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 177:551–558CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  • Sandra Silvina Aliscioni
    • 1
    • 2
    • 3
    Email author
  • Marina Gotelli
    • 2
    • 3
  • Juan Pablo Torretta
    • 2
    • 3
  1. 1.Instituto de Botánica Darwinion (IBODA)San IsidroArgentina
  2. 2.Facultad de Agronomía, Cátedra de Botánica GeneralUniversidad de Buenos AiresBuenos AiresArgentina
  3. 3.Consejo Nacional de Investigaciones Científicas y TécnicasBuenos AiresArgentina

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