Elsevier

Flora

Volume 270, September 2020, 151649
Flora

A revision of the Ceratozamia miqueliana (Zamiaceae) species complex based on analyses of leaflet anatomical characters

https://doi.org/10.1016/j.flora.2020.151649Get rights and content

Highlights

  • Leaflet anatomy for the C. miqueliana complex described for the first time.

  • The confusion of C. becerrae with C. zoquorum has been solved.

  • Leaflet anatomy conforms C. becerrae as a good species.

  • Plant anatomy has proved useful for solving conflicting molecular data.

Abstract

The Ceratozamia miqueliana species complex consists of six closely related species that exhibit similar gross morphology, but a wide range of leaflet shape from widely obovate in C. euryphyllidia and C. hondurensis to oblanceolate in C. zoquorum. However, despite the clear leaflet size variation, the taxon delimitation within the complex has been suggested to be uncertain when considering other traits, giving rise to doubts about the taxonomic validity of taxa, particularly of C. becerrae. Previous studies have shown that anatomical traits might be effective diagnostic characters to delimitate closely related cycad species. This study reviewed the anatomical variation of the Ceratozamia miqueliana species complex. We provide taxonomic treatment in the basis of anatomical trait variation. Although the six species occupy relatively mesic environments in tropical rainforest habitats, we found that some species exhibited leaflet anatomical traits associated to water stressed environments, suggesting historical adaptation to xeric conditions. The anatomical trait variation presented in this study agrees with a recent molecular phylogenetic study, clears up doubts on species relationships in the C. miqueliana complex, and validates the taxonomic recognition of C. becerrae.

Introduction

Wendland (1854) described Ceratozamia miqueliana H. Wendl. from a sterile specimen from an unknown locality. Fortunately, Thiselton-Dyer’s (1883) excellent illustration showing leaflet and strobili details enabled its rediscovery in southern Veracruz (Vovides et al., 1983). Ceratozamia miqueliana bears leaves with obovate to broadly oblanceolate leaflets and erect megastrobilus. Since then, further localities of this species have been found in Tabasco and northern Chiapas (Pérez-Farrera et al., 2009). Furthermore, five additional species within the C. miqueliana complex have since been described: (Fig. 1). Ceratozamia becerrae Pérez-Farr., Vovides & Schutzman (Tabasco, Mexico) with oblong to oblanceolate leaflets and erect megastrobilus; C. euryphyllidia Vázq.Torres, Sabato & Stevenson (southern Veracruz and Oaxaca, Mexico) with widely obovate to broadly oblanceolate leaflets and erect megastrobilus; C. hondurensis J.L. Haynes, Whitelock, Schutzman & R.S. Adams (Honduras) with widely obovate to broadly oblanceolate leaflets and erect megastrobilus; C. santillanii Pérez-Farr. & Vovides and C. zoquorum Pérez-Farr., Vovides & Iglesias both bearing oblong to oblanceolate leaflets but C. zoquorum bears a decumbent megastrobilus at maturity and glaucous leaflets when emergent (both species are from northern Chiapas, Mexico). We consider these five species as the Ceratozamia miqueliana species complex, hereafter referred as the ‘Miqueliana complex’, and the leaflet types as ‘miquelianoid’. Species within the Miqueliana complex have been described in consideration of the morphological variation of leaves and leaflets, in which, for example, ‘miquelianoid’ leaflets vary in width, C. euryphyllidia and C. hondurensis bearing the widest and C. zoquorum the narrowest. Yet, a recent taxonomic controversy has arisen within the complex: Ceratozamia becerrae Pérez-Farr., Vovides & Schutzman has recently been synonymized with C. zoquorum Pérez-Farr., Vovides & Iglesias by Martínez-Domínguez et al. (2017). Such proposal was based on the absence of overall variation among morphological traits, and the lack of variation in the internal transcribed spacer (ITS) of the ribosomal DNA. However, such study ignored previous morphological and molecular evidences (González and Vovides, 2002, 2012; Vovides et al., 2004a, 2004b, 2004c and illustration therein). Notably, Martínez-Domínguez et al.(2017) did not find the decumbent cone as a diagnostic character, but this is likely because the authors did not differentiate between newly emerging cones, which will always be erect in both species, and maturing cones, which will be decumbent only in C. zoquorum. Therefore, the decision to synonymize C. becerrae with C. zoquorum might be biased with arbitrary criteria. Such criteria might be problematic for the taxonomy of cycads, and in textual words of Kadereit et al. (2012) “Lumping similar species into single taxa would therefore produce polyphyletic taxa, which is unacceptable to any taxonomist who believes that species should reflect evolutionary history”. Thus, it is important to make a revision on the characteristics that define and delimitate the ‘Miqueliana’ species.

Geographically, the five Mexican species of the Miqueliana complex (C. becerrae, C. euryphyllidia, C. miqueliana, C. santillanii and C. zoquorum) occur in mesic forests with high annual precipitation, according to the bioclimatic layer bio12 in www.worldclim.org (Hijmans et al., 2005) (Fig. 1). Their populations lie in different areas within the Pleistocene floristic refugia identified by Wendt (1987). Ceratozamia miqueliana is also present in the Los Tuxtlas refuge, whilst C. hondurensis is present only in the Izabal refuge of Wendt (1987) in Honduras. Ceratozamia becerrae grows on Tertiary sedimentary rock on a calcareous base, whilst the substrate of the C. zoquorum habitat is late/upper Cretaceous on calcareous substrate. Ceratozamia santillanii and C. zoquorum are found only on karstic topography, but C. miqueliana grows on basaltic rock and clay soils (Ferrusquía-Villafranca, 1998; Pérez-Farrera et al., 2009) occupying the herbaceous strata under shade in evergreen tropical rain forest. In this study, the precise locality information of the populations of all species are omitted in order to prevent poaching of these rare and endangered cycads.

Leaflet anatomical studies have been demonstrated useful in the delimitation of closely related species within cycads. For example, previous molecular phylogenetic methods placed C. brevifrons Miq. along with C. mexicana on an unresolved polytomic clade (González and Vovides, 2012), suggesting a synonymous status of the two taxa; but a consequent study based on morphology and anatomical trait variation made clear distinction between the two species (Vovides et al., 2012). Likewise, a morphology and leaflet anatomy study has helped to define the Ceratozamia norstogii D.W.Stev. complex (Pérez-Farrera et al., 2014). When combined with genetic methods, morphological and anatomical traits were useful to reveal a putative hybrid origin of Z. katzeriana (Regel) E. Rettig by Pérez-Farrera et al. (2016), whilst the concept of Dioon sonorense (De Luca, Sabato & Vázq.Torres) Chemnick, T.J.Greg. & Salas-Mor. was found to consist of two taxa (Gutiérrez-Ortega et al., 2018b). Furthermore, Acuña-Castillo and Marín-Méndez (2012) studied the leaflet anatomy of Z. neurophyllidia and Z. fairchildiana and found differences in anatomical traits between the two species, but indicating xerophytic ancestry in common. Leaflet anatomical studies have been also useful at higher taxonomic rank comparisons. Tang et al. (2004) described the leaflet anatomy of ten cycad species from six genera, and found that the pinna venation and anatomy to be consistent with the Stevenson (1992) classification of Zamiaceae. All these above publications have demonstrated the great importance of anatomical trait variation for cycad taxonomy. Therefore, this study aims to describe the anatomical variation among the species of the Miqueliana complex.

Section snippets

Sampling

The specimens used were obtained from the Clavijero Botanic Garden living collections cultivated under uniform conditions for over 12 years, thus avoiding phenotypic variation. Double stained permanent preparations of the middle area of leaflets taken from the middle portion of mature leaves were used for descriptions, measurements and photomicrography. Two individuals of the five Mexican species were used to obtain leaflet material (Table 1). One species, C. hondurensis was represented by one

Observations

The leaflet anatomy in transverse section (TS) of Ceratozamia zoquorum has four layers of girder sclerenchyma connecting the vascular bundle and a lignified adaxial hypodermis whereas in C. becerrae the adaxial hypodermis is absent and girder sclerenchyma mostly absent or a single layer of a few cells not reaching the vascular bundle. In C. euryphyllidia, C. hondurensis and C. miqueliana girder sclerenchyma and hypodermis are absent (Table 3, Fig. 2). In C. euryphyllidia and C. miqueliana the

Morphogeographic evidence

All taxa in the Miqueliana complex show obvious morphological differences among them. Ceratozamia becerrae has oblong or very rarely oblanceolate leaflets with inter-leaflet distance 5.3–12.8 cm and erect megastrobilus with peduncles 2–3 cm long. In C. zoquorum leaflets are very coriaceous, long oblanceolate with inter-leaflet distance 4.8–9.5 cm, the leaves emerging circinate and these are pruinose and decumbent megastrobilus (see illustrations in Vovides et al., 2004a, 2004b, 2004c). The

Conclusion

Anatomical trait variation within the Miqueliana species complex confirm with confidence that the taxa C. becerrae, C. euryphyllidia, C. hondurensis, C. miqueliana, C. santillanii and C. zoquorum constitute well-defined species. It implies that C. becerrae should be recognized as a distinct species easily distinguishable from C. zoquorum morphologically and anatomically. Also, this study reinforces the utility of anatomical techniques for the taxonomic recognition of cycads, and shows that a

CRediT authorship contribution statement

M.A. Pérez-Farrera: Investigation, Formal analysis.

J.S. Gutérrez-Ortega: Writing original draft, Formal analysis, Bioclimatic data, Visulaization.

S. Avendaño: Data curation and Herbarium specimens.

A. Medina-Villarreal: Resources.

J. González-Astorga: Data analysis.

S. Galicia: Visualization, Histological preparations, Photomicrography.

Declaration of Competing Interest

None.

Acknowledgements

APV acknowledges several CONACYT finances over the years, especially project no. CB 2011-169468-B for the partial funding of this research. Also, the Jardín Botánico Fco. J. Clavijero of the Instituto de Ecología, A.C. that holds the Mexican National Collection of Living Cycads where most of the leaflet material was taken. MAPF thanks anonymous donors to Montgomery Botanical Center for financial support. JSGO acknowledges the Japan Society for the Promotion of Science (Grant-in-Aid No. 18F18076

References (42)

  • M.A. Pérez-Farrera et al.

    A new species of Ceratozamia (Zamiaceae) from Chiapas, Mexico

    Bot. J. Linn. Soc.

    (2001)
  • C. Schwarzer et al.

    Parallel adaptive responses to abiotic but not biotic conditions after cryptic speciation in European peat moss Sphagnum magellanicum Brid

    Perspect. Plant Ecol. Evol. Syst.

    (2017)
  • R. Acuña-Castillo et al.

    Some aspects of the foliar anatomy of two Zamia species from Costa Rica: Z. fairchildiana L.D. Gómez and Z. neurophyllidia D.W. Stev

  • D.A. Baum et al.

    Choosing among alternative “phylogenetic” species concepts

    Syst. Bot.

    (1995)
  • M. Calonje et al.

    A time-calibrated species tree phylogeny of the new world cycad genus Zamia L. (Zamiaceae, Cycadales)

    Int. J. Plant Sci.

    (2019)
  • B. Dauphin et al.

    A worldwide molecular phylogeny provides new insight on cryptic diversity within the moonworts (Botrychium s. S., Ophioglossaceae)

    Syst. Bot.

    (2017)
  • K. De Queiroz

    Species concepts and species delimitation

    Syst. Biol.

    (2007)
  • E.C. Dudley

    Adaptive radiation in the Melastomataceae along an altitudinal gradient in Peru

    Biotropica

    (1978)
  • W.T. Thiselton-Dyer

    Cycadaceae. Biologia Centrali-Americana 3: 190–195

    (1883)
  • I. Ferrusquía-Villafranca

    Geología de México: Una sinopsis

  • D. González et al.

    Low intralineage divergence in the genus Ceratozamia Brongn. (Zamiaceae) detected with nuclear ribosomal DNA ITS and chloroplast DNA trnL-F non-coding region

    Syst. Bot.

    (2002)
  • D. González et al.

    A modification to the SCAR (Sequence Characterized Amplified Region) method provides phylogenetic insights within Ceratozamia (Zamiaceae)

    Revista Mexicana de Biodiversidad

    (2012)
  • A. Graham

    Late Cenozoic evolution of tropical lowland vegetation in Veracruz, Mexico

    Evolution

    (1976)
  • J.S. Gutiérrez-Ortega et al.

    Aridification as a driver of biodiversity: a case study for the cycad genus Dioon (Zamiaceae)

    Ann. Bot.

    (2018)
  • J.S. Gutiérrez-Ortega et al.

    Considering evolutionary processes in cycad conservation: identification of evolutionarily significant units within Dioon sonorense (Zamiaceae) in northwestern Mexico

    Conserv. Genet.

    (2018)
  • Ø. Hammer et al.

    PAST-palaeontological statistics, ver. 1.89

    Palaeontol. Electron.

    (2001)
  • J.L. Haynes et al.

    A new endemic Ceratozamia from Honduras (Cycadales: Zamiaceae)

    Cycad Newsletter

    (2008)
  • R.J. Hijmans et al.

    Very high resolution interpolated climate surfaces for global land areas

    Int. J. Climatol.

    (2005)
  • G. Kadereit et al.

    Cryptic taxa should have names: reflections in the glasswort genus Salicornia (Amaranthaceae)

    Taxon

    (2012)
  • E.S. López-Hernández

    La vegetación y la flora de la Sierra de Tabasco

    (1994)
  • R. López-Mendoza

    Tipos de vegetación y su distribución en el estado de Tabasco y norte de Chiapas

    (1980)
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