Skip to main content
Log in

Epidermal crystals in Acalypha (Euphorbiaceae, Acalyphoideae) as a new taxonomic trait of the genus

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

The occurrence of epidermal crystals in the species of the genus Acalypha (Euphorbiaceae, Acalyphoideae) is described and analyzed. The epidermal surface of 190 Acalypha specimens, belonging to 110 species and subspecies, was studied with a scanning electron microscope (SEM), and the elemental composition of the found crystals was examined using energy-dispersive X-ray spectroscopy (EDS). The results show that 96.4 % of the studied species have epidermal crystals, mainly located on the leaf surface, but also on the bracts and flowers. The crystals exhibit significant variation, and four types of crystals are recognized: prismatic, styloids, stellate, and druses, which are, respectively, designated with Ac, Bc, Cc and Dc letters. We have not found any reference to stellate crystals in the angiosperm morphological or anatomical literature, and druses are observed and described under SEM in Acalypha for the first time. The elemental composition of the crystals shows that all of them exhibit typical peaks of calcium. We discuss the possible taxonomic importance of crystals, due to the association that some of these types of crystals have with groups of closely morphologically related species. We have not found a relation between the presence or the type of crystals and the habitat or distribution of the species that present them. We do not know other genera of Euphorbiaceae where the presence of crystals is so widespread, so we propose that they should be considered as a distinctive feature of this genus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Arnott HJ (1982) Three systems of biomineralization in plants with comments on the associated organic matrix. In: Nancollas GH (ed) Biological mineralization and demineralization. Springer, Berlin, pp 199–218

    Chapter  Google Scholar 

  • Aworinde DO, Nwoye DU, Jayeola AA, Olagoke AO, Ogundele AA (2009) Taxonomic significance of foliar epidermis in some members of Euphorbiaceae family in Nigeria. Res J Bot 4:17–28. https://doi.org/10.3923/rjb.2009.17.28

    Article  Google Scholar 

  • Bacigalupo NM (2005) Acalypha. In: Burkart A, Bacigalupo NM (eds) Flora ilustrada de Entre Ríos (Argentina), vol. 6(4). Instituto Nacional de Tecnología Agropecuaria, Buenos Aires, pp 170–176

    Google Scholar 

  • Cardiel JM (1995) Cristales foliares en Acalypha L. (Euhorbiaceae). Anales Jard Bot Madrid 53:181–189

    Google Scholar 

  • Cardiel JM, Montero Muñoz I (2018) Synopsis of Acalypha (Euphorbiaceae) of West Tropical Africa, including Cameroon, Chad, Equatorial Guinea, Gabon, and São Tomé and Príncipe. Pl Syst Evol 304:93–110. https://doi.org/10.1007/s00606-017-1453-4

    Article  Google Scholar 

  • Cardiel JM, Muñoz-Rodríguez P (2012) Synopsis of Acalypha (Euphorbiaceae) of continental Ecuador. PhytoKeys 17:1–17. https://doi.org/10.3897/phytokeys.17.3190

    Article  Google Scholar 

  • Cardiel JM, Muñoz-Rodríguez P (2013) Acalypha carrascoana Cardiel (Euphorbiaceae) novelty for the flora of Mexico. Bot Complut 37:53–56. https://doi.org/10.5209/rev_BOCM.2013.v37.42269

    Article  Google Scholar 

  • Cardiel JM, Muñoz-Rodríguez P (2015) Synopsis of Acalypha (Euphorbiaceae) of Argentina, Paraguay, and Uruguay. Ann Missouri Bot Gard 101:384–405. https://doi.org/10.3417/2014006

    Article  Google Scholar 

  • Cardiel JM, Muñoz-Rodríguez P, Muñoz Garmendia F (2013) Revised taxonomy and nomenclature of Acalypha sect. Communes (Euphorbiaceae), a complex group of species widespread in the north of the Southern Cone. Taxon 62:1295–1303. https://doi.org/10.12705/626.11

    Article  Google Scholar 

  • Cardiel JM, Montero Muñoz I, Sancho García I (2018) Three new species of Acalypha (Euphorbiaceae, Acalyphoideae) from Argentina, Bolivia, Brazil and Paraguay. Phytotaxa 356:158–166. https://doi.org/10.11646/phytotaxa.356.2.5

    Article  Google Scholar 

  • Cardiel JM, Muñoz-Rodríguez P, Dorda E, Pardo de Santayana M (2020) Acalypha taxonomic information system. Available at: http://www.acalypha.es. Accessed 8 Feb 2020

  • Cervantes-Martinez T, Horner HT, Palmer RG, Hymowitz T, Brown AHD (2005) Calcium oxalate crystals macropatterns in leaves of species from groups Glycine and Shuteria (Glycininae; Phaseoleae; Papilionoideae; Fabaceae). Canad J Bot 83:1410–1421. https://doi.org/10.1139/b05-119

    Article  CAS  Google Scholar 

  • Chavarri B, León WJ (2005) Estudio anatómico del xilema secundario en siete especies de la subfamilia Acalyphoideae (Euphorbiaceae) en Venezuela. Acta Bot Venez 28:233–256

    Google Scholar 

  • Committee IAWA (1989) IAWA list of microcopic features for hardwood identification. IAWA Bull 10:219–332

    Article  Google Scholar 

  • De Pompert MG (1989) Estudio morfo-anatómico de dos especies de Sapium (Euphorbiaceae). Bonplandia 6:197–210. https://doi.org/10.30972/bon.62-31516

    Article  Google Scholar 

  • De-Paula OC, Graças Sajo M (2011) Morphology and development of anthers and ovules in Croton and Astraea (Euphorbiaceae). Nordic J Bot 29:505–511. https://doi.org/10.1111/j.1756-1051.2011.01072.x

    Article  Google Scholar 

  • Di Sapio OA, Gattuso MA (2013) Caracteres morfoanatómicos y micrográficos de la corteza de Croton urucurana Baillon (Euphorbiaceae). Dominguezia 29:7–16

    Google Scholar 

  • Doaigey AR (1991) Occurrence, type, and location of calcium oxalate crystals in leaves and stems of 16 species of poisonous plants. Amer J Bot 78:1608–1616. https://doi.org/10.1002/j.1537-2197.1991.tb14527.x

    Article  CAS  Google Scholar 

  • Essiett UA, Etukudo IS (2012) Leaf epidermal studies of three species of Acalypha Linn. (Euphorbiaceae). Advances Appl Sci Res 3:3185–3199

    Google Scholar 

  • Fiser Pecnikar Z, Kulju KKJ, Sierra SEC, Baas P, Van Welzen PC (2012) Leaf anatomy of Mallotus and the related genera Blumeodendron and Hancea (Euphorbiaceae sensu stricto). Bot J Linn Soc 169:645–676. https://doi.org/10.1111/j.1095-8339.2012.01227.x

    Article  Google Scholar 

  • Franceschi VR, Horner HT (1980) Calcium oxalate crystals in plants. Bot Rev 46:361–427

    Article  CAS  Google Scholar 

  • Franceschi VR, Nakata PA (2005) Calcium oxalate in plants: formation and function. Annual Rev Pl Biol 56:41–71. https://doi.org/10.1146/annurev.arplant.56.032604.144106

    Article  CAS  Google Scholar 

  • Hayden WJ, Hayden SM (2000) Wood anatomy of Acalyphoideae (Euphorbiaceae). IAWA J 21:213–235

    Article  Google Scholar 

  • Hazra K, Dutta S, Ghosal S, Paria S, Rao MM (2019) Phytopharmacognostic evaluation of plant Euphorbia hirta L. Int J Herb Med 7:7–15

    Google Scholar 

  • He H, Bleby TM, Veneklaas EJ, Lambers H, Kuo J (2012a) Morphologies and elemental compositions of calcium crystals in phyllodes and branchlets of Acacia robeorum (Leguminosae: Mimosoideae). Ann Bot (Oxford) 109:887–896. https://doi.org/10.1093/aob/mcs004

    Article  CAS  Google Scholar 

  • He H, Bleby TM, Veneklaas EJ, Lambers H, Kuo J (2012b) Precipitation of calcium, magnesium, strontium and barium in tissues of four Acacia species (Leguminosae: Mimosoideae). PLoS ONE 7:1–12. https://doi.org/10.1371/journal.pone.0041563

    Article  CAS  Google Scholar 

  • Horner HT, Wanke S, Samain M-S (2009) Evolution and systematic value of leaf crystal macropatterns: a phylogenetic approach in the genus Peperomia (Piperaceae). Int J Pl Sci 170:343–354

    Article  Google Scholar 

  • Kabouw P, Van Welzen PC, Baas P, Van Heuven BJ (2008) Styloid crystals in Claoxylon (Euphorbiaceae) and allies (Claoxylinae) with notes on leaf anatomy. Bot J Linn Soc 156:445–457. https://doi.org/10.1111/j.1095-8339.2007.00757.x

    Article  Google Scholar 

  • Kadiri AB, Adeniran S (2016) Study of anatomy of the genus Hura L. (Euphorbiaceae). Ife J Sci 18:413–426

    Google Scholar 

  • Kadiri AB, Olowokudejo JD, Ogundipe OT (2009) Leaf epidermis morphology of west African species of the genus Acalypha (Euphorbiaceae). Bot Lithuan 15:65–78

    Google Scholar 

  • León WJ, Chavarri BN (2006) Anatomía xilemática del tallo de 8 especies de la subfamilia Euphorbioideae (Euphorbiaceae) en Venezuela. Revista Fac Agron Univ Nac La Plata 106:1–12

    Google Scholar 

  • Lersten NR, Horner HT (2009) Crystal diversity and macropatterns in leaves of Oleaceae. Pl Syst Evol 282:87–102. https://doi.org/10.1007/s00606-009-0209-1

    Article  CAS  Google Scholar 

  • Lersten NR, Horner HT (2011) Unique calcium oxalate “duplex” and “concretion” idioblasts in leaves of tribe Naucleeae (Rubiaceae). Amer J Bot 94:1–11. https://doi.org/10.3732/ajb.1000247

    Article  Google Scholar 

  • Levin GA, Steinmann VW, Sagun VG (2005) Phylogeny and biogeography of Acalypha (Euphorbiaceae). In: XVII international botanical congress. Vienna, Austria, Europe. Abstracts. Robidruck, Vienna, p 68

  • Maciel-Júnior L, Cardiel JM, Rossine Y, de Melo AL (2020) An update on Acalypha inselbergensis Cardiel & I. Montero (Euphorbiaceae): a recently described species from Brazil. Check List 16:957–961. https://doi.org/10.15560/16.4.957

    Article  Google Scholar 

  • Metcalfe CR (1983) Secreted mineral substances. Crystals. In: Metcalfe CR, Chalk L (eds) Anatomy of the dicotyledons 2, 2nd edn. Oxford University Press, London, pp 82–91

    Google Scholar 

  • Metcalfe CR, Chalk L (1950) Anatomy of the dicotyledons 2. Oxford University Press, London

    Google Scholar 

  • Murillo J (2002) Anatomía foliar de la subtribu Conceveibinae (Euphorbiaceae). Revista Biol Trop 50:9–20

    Google Scholar 

  • Oladipo OT, Olanrewaju SO, Akinloye JA (2015) Comparative epidermal morphology and petiole anatomical study of Acalypha hispida Burm.F. and Acalypha wilkesiana Muell. Arg. varieties (Euphorbiaceae). FUTA J Res Sci 11:315–322

    Google Scholar 

  • Pax FA, Hoffmann K (1924) Acalypha. In: Engler A (ed) Das Pflanzenreich (Heft 85) IV. 147. xvi. Wilhelm Engelmann, Leipzig, pp 1–231

  • Prychid CJ, Rudall PJ (1999) Calcium oxalate crystals in Monocotyledons: a review of their structure and systematics. Ann Bot (Oxford) 84:725–739. https://doi.org/10.1006/anbo.1999.0975

    Article  CAS  Google Scholar 

  • Raju VS, Rao PN (1977) Variation in the structure and development of foliar stomata in the Euphorbiaceae. Bot J Linn Soc 75:69–97. https://doi.org/10.1111/j.1095-8339.1977.tb01479.x

    Article  Google Scholar 

  • Riina R, Cumbicus N, Feiro AC, Cerón CE, Strozi RM, Berry PE (2015) A new species of dragon’s blood Croton (Euphorbiaceae) from South America with singular inflorescences. Weebia 70:187–192. https://doi.org/10.1080/00837792.2015.1020129

    Article  Google Scholar 

  • Rodríguez-Morales D, Aguirre A, Coates R, Díaz-Castellano C, Angeles G (2016) Structure and histology of extrafloral nectaries of tropical species in a Mexican rain forest. Biosci J 32:730–739. https://doi.org/10.14393/BJ-v32n3a2016-30416

    Article  Google Scholar 

  • Roth I, Lindorf H (2002) South American medicinal plants: botany, remedial properties and general use. Springer, Heidelberg

    Book  Google Scholar 

  • Rudall PJ (2007) Anatomy of flowering plants. An introduction to structure and development, 3rd edn. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Sagun VG, Levin GA, Van Welzen PC (2010) Revision and phylogeny of Acalypha (Euphorbiaceae) in Malesia. Blumea 55:21–60. https://doi.org/10.3767/000651910X499141

    Article  Google Scholar 

  • Sá-Haiad B, Serpa-Ribeiro ACC, Barbosa CN, Pizzini D, Leal D, Senna-Valle L, Santiago-Fernandes LDR (2009) Leaf structure of species from three closely related genera from tribe Crotoneae Dumort. (Euphorbiaceae s.s., Malpighiales). Pl Syst Evol 283:179–202. https://doi.org/10.1007/s00606-009-0229-x

    Article  Google Scholar 

  • Seebaluck R, Gurib-Fakim A, Mahomoodally F (2015) Medicinal plants from the genus Acalypha (Euphorbiaceae). A review of their ethnopharmacology and phytochemistry. J Ethnopharmacol 159:137–157. https://doi.org/10.1016/j.jep.2014.10.040

    Article  CAS  PubMed  Google Scholar 

  • Sharma V, Pracheta (2013) Microscopic studies and preliminary pharmacognostical evaluation of Euphorbia neriifolia L. leaves. Indian J Nat Prod Resour 4:348–357

    Google Scholar 

  • Solerender H (1908) Systematic anatomy of the dicotyledons: a handbook for laboratories of pure and applied 2. Clarendon Press, Oxford

    Google Scholar 

  • Steinmann VW, Levin GA (2003) The copperleaf conundrum: molecular and morphological data appear irreconcilable in Acalypha (Euphorbiaceae). Botany 2003, annual meeting of Botanical Society of America, Mobile, Alabama, USA. Abstracts, p 96

  • Thakur HA, Patil DA (2011) Petiolar Anatomy of some unstudied Euphorbiaceae. J Phytol 2:54–59

    Google Scholar 

  • Thiers B (2019) Index Herbariorum: a global directory of public herbaria and associated staff. The New York Botanical Garden’s Virtual Herbarium, Bronx. Available at: http://sweetgum.nybg.org/science/ih. Accessed 8 Jan 2020

  • Tokuoka T (2007) Molecular phylogenetic analysis of Euphorbiaceae sensu stricto based on plastid and nuclear DNA sequences and ovule and seed character evolution. J Pl Res 120:511–522. https://doi.org/10.1007/s10265-007-0090-3

    Article  CAS  Google Scholar 

  • Vitarelli NC, Riina R, Caruzo MBR, Cordeiro I, Fuertes-Aguilar J, Meira RMSA (2015) Foliar secretory structures in Crotoneae (Euphorbiaceae): diversity, anatomy and evolutionary significance. Amer J Bot 102:833–847. https://doi.org/10.3732/ajb.1500017

    Article  Google Scholar 

  • Webb MA (1999) Cell-mediated crystallization of calcium oxalate in plants. Pl Cell 11:751–761. https://doi.org/10.1105/tpc.11.4.751

    Article  CAS  Google Scholar 

  • Wurdack KJ, Davis CC (2009) Malpighiales phylogenetics: gaining ground on one of the most recalcitrant clades in the angiosperm tree of life. Amer J Bot 96:1551–1570. https://doi.org/10.3732/ajb.0800207

    Article  Google Scholar 

  • Wurdack KJ, Hoffmann P, Chase MW (2005) Molecular phylogenetic analysis of uniovulate Euphorbiaceae (Euphorbiaceae sensu stricto) using plastid rbcL and trnL-F DNA sequences. Amer J Bot 92:1397–1420. https://doi.org/10.3732/ajb.92.8.1397

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We kindly thank the curators and staff of the herbaria mentioned for facilitating the study of their specimens; Dra. Ricarda Riina of the Real Jardín Botánico of Madrid, Dra. Renata Maria Strozi Alves Meira, of the Universidade Federal de Viçosa, Minas Gerais, Brazil, and Narah Costa Vitarelli, of the Instituto Federal de Educação, Ciência e Tecnologia do Sudeste de Minas Gerais, Brazil, for their helpful comment about the stellate crystals; and Esperanza Salvador Rueda and the staff of the SEM laboratory of the Servicio Interdepartamental de Investigación (SIDI-UAM) for his meticulous technical work. Finally, we express our gratitude to Lucía Cardiel Celis for the careful grammatical review and to the editor and reviewers for their suggestions and helpful comments.

Funding

This study was funded by Gobierno de España, through the research Project EUI 2008-0388, and by the Universidad Autónoma de Madrid (Spain) and the Regional Government (Comunidad de Madrid), through the research project CCG07-UAM/AMB-1453. This research has received support from the SYNTHESYS Project (http://www.synthesys.info/; FR-TAF 6307, DE-TAF 3319, and SE-TAF 5590) that is financed by the European Community Research Infrastructure Action under the FP7 Ideas: European Research Council “Capacities” Program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to José María Cardiel.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

The authors declare the compliance of ethical standards.

Additional information

Handling Editor: Jürg Schönenberger.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cardiel, J.M., Montero-Muñoz, I., Ortúñez, E. et al. Epidermal crystals in Acalypha (Euphorbiaceae, Acalyphoideae) as a new taxonomic trait of the genus. Plant Syst Evol 306, 83 (2020). https://doi.org/10.1007/s00606-020-01711-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00606-020-01711-6

Keywords

Navigation