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Ceratozamia Aurantiaca (Zamiaceae): a New Cycad Species from the Northern Rainforests of Oaxaca, Mexico

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Ceratozamia Aurantiaca (Zamiaceae): a New Cycad Species from the Northern Rainforests of Oaxaca, Mexico Article Ceratozamia aurantiaca (Zamiaceae): A New Cycad Species from the Northern Rainforests of Oaxaca, Mexico Miguel Angel Pérez-Farrera 1,2,*, José Said Gutiérrez-Ortega 3,* , Jody L. Haynes 4 , Jeff Chemnick 5, Silvia H. Salas-Morales 6, Michael Calonje 7 and Andrew P. Vovides 8 1 Laboratorio de Ecología Evolutiva, Herbario Eizi Matuda, Instituto de Ciencias Biológicas, Universidad de Ciencias y Artes de Chiapas, Tuxtla Gutiérrez 29039, Mexico 2 Facultad de Ciencias Naturales, Universidad Autónoma de Querétaro, Ave. De las Ciencias s/n, Juriquilla, Santa Rosa Jáuregui, Querétaro 76230, Mexico 3 Institute for Excellence in Educational Innovation, Chiba University, Chiba 263-8522, Japan 4 Fairchild Tropical Botanic Garden, Coral Gables, FL 33156, USA; [email protected] 5 Ganna Walska Lotusland, Santa Barbara, CA 93108, USA; [email protected] 6 Sociedad para el Estudio de los Recursos Bióticos de Oaxaca, San Sebastián Tutla, Oaxaca 71246, Mexico; [email protected] 7 Montgomery Botanical Center, Coral Gables, FL 33156, USA; [email protected] 8 Red de Biología Evolutiva, Instituto de Ecología, A.C., Xalapa 91070, Mexico; [email protected] * Correspondence: [email protected] (M.A.P.-F.); [email protected] (J.S.G.-O.) Abstract: Ceratozamia aurantiaca, a new cycad species from Oaxaca, Mexico, is described. The new species is endemic to lowland karst tropical rainforests of the northern mountains (Sierra Norte region). This species is related to C. subroseophylla and C. robusta, together considered part of the C. robusta species complex due to their shared characteristics: robust, upright trunk; large and Citation: Pérez-Farrera, M.A.; long leaves with densely armed petioles and linear to subfalcate leaflets; and large megastrobili. Gutiérrez-Ortega, J.S.; Haynes, J.L.; Ceratozamia aurantiaca, as the epithet suggests, is easily distinguished from other species by the orange Chemnick, J.; Salas-Morales, S.H.; color of its emerging leaves, a trait unique in the genus. Additionally, C. aurantiaca is distinguished Calonje, M.; Vovides, A.P. Ceratozamia aurantiaca (Zamiaceae): A New Cycad from C. subroseophylla and C. robusta by having significantly shorter petioles, wider spacing between Species from the Northern leaflets, and wider median leaflets. The taxonomic recognition of this species represents a step toward Rainforests of Oaxaca, Mexico. clarifying species delimitation in the C. robusta complex. Taxonomy 2021, 1, 243–255. https:// doi.org/10.3390/taxonomy1030018 Keywords: cycads; botanic gardens; endangered species; morphological analyses; new species; Mexico Academic Editor: Xian-Chun Zhang Received: 4 August 2021 1. Introduction Accepted: 18 August 2021 The cycad genus Ceratozamia Brongn. (Zamiaceae) currently comprises 33 species from Published: 19 August 2021 Mexico, Guatemala, Belize, and Honduras, with all but three endemic to Mexico [1]. Most species are represented by one to a few narrowly distributed populations separated by a few Publisher’s Note: MDPI stays neutral to several kilometers, generally inhabiting tropical evergreen forest, oak forest, or tropical with regard to jurisdictional claims in montane cloud forest [2]. In Ceratozamia, species that are closely related phylogenetically published maps and institutional affil- also tend to exhibit geographic proximity and similar morphology [3], which are criteria iations. considered as proxy when testing species delimitation. The species definition within the genus has traditionally been based on morpho-geographic criteria, such that each species is represented by one or more geographically close populations that share morphological characteristics [4,5]. Even so, species delimitation among closely related species has been a Copyright: © 2021 by the authors. constant challenge in Ceratozamia [2,6,7]. Licensee MDPI, Basel, Switzerland. Recent reviews of the genus have proposed the recognition of species complexes, This article is an open access article which are groups of species with high morphological resemblance [2,8]. Belonging to a distributed under the terms and species complex in Ceratozamia implies that it can be difficult to correctly identify a member conditions of the Creative Commons Attribution (CC BY) license (https:// taxon within the complex if detailed information about its origin in the wild is unknown. creativecommons.org/licenses/by/ The C. robusta species complex has been considered one of the most taxonomically difficult 4.0/). groups in the genus [2] (Figure1). Plants belonging to this species complex are easily Taxonomy 2021, 1, 243–255. https://doi.org/10.3390/taxonomy1030018 https://www.mdpi.com/journal/taxonomy Taxonomy 2021, 1, FOR PEER REVIEW 2 Taxonomy 2021, 1 244 ber taxon within the complex if detailed information about its origin in the wild is un- known. The C. robusta species complex has been considered one of the most taxonomically difficult groups in the genus [2] (Figure 1). Plants belonging to this species complex are recognizedeasily recognized by their by robust their epigeousrobust epigeous trunks, largetrunks, robust large cones, robust large cones, leaves, large and leaves, petioles and thatpetioles are densely that are armed densely with armed prickles—a with setprickles of traits—a distinct set of traits in the distinct genus. Increasedin the genus. interest In- increased cycads interest in the latein cycads 20th centuryin the late led 20 toth thecentury discovery led to ofthe populations discovery of of populationsC. robusta Miq. of C. inrobusta the states Miq. ofin Chiapas,the states Oaxaca,of Chiapas, and Oaxaca, Veracruz and (Mexico), Veracruz as (Mexico well as), inas well Guatemala as in Guate- and Belizemala and (Figure Belize1). Although(Figure 1). all Although populations all populations from these regionsfrom these share regions the aforementioned share the afore- suitementioned of morphological suite of morphological characteristics, characterist a highics, level a high of variation level of variation among populations among popula- of C.tions robusta of C. sensu robusta lato sensuwas lato previously was previously noted [5 noted] and has[5] and only has been only carefully been carefully examined exam- in recentined in years recent [7, 9years,10]. [7,9,10]. FigureFigure 1. 1.Distribution Distribution map map of of the the known known populations populations of ofCeratozamia Ceratozamia robusta robustaspecies species complex. complex. Black Black circles surrounded by a dotted line indicate the occurrence of populations of C. robusta, as currently circles surrounded by a dotted line indicate the occurrence of populations of C. robusta, as currently circumscribed. The star symbol indicates the neotype locality of C. robusta (Parque Nacional Cañón circumscribed. The star symbol indicates the neotype locality of C. robusta (Parque Nacional Cañón del Sumidero, Chiapas, Mexico). Ceratozamia subroseophylla, previously considered as C. robusta, has delbeen Sumidero, recorded Chiapas, in two areas Mexico). in SantiagoCeratozamia Tuxtla, subroseophylla Veracruz, ,Mexico. previously The consideredputative new as C.species robusta (herein, has beennamed recorded Ceratozamia in two aurantiaca areas in; Santiago see results Tuxtla,) occurs Veracruz, in two localities Mexico. Thein the putative Sierra Norte new speciesregion, (hereinOaxaca, namedMexico;Ceratozamia these populations aurantiaca have; see been results) long occurs considered in two localitiesas C. robusta in the. Green Sierra color Norte scale region, indicates Oaxaca, the Mexico;elevation these in meters populations above havesea level been (m long a.s.l. considered) as recorded as C.in the robusta raster. Green layers color of 30 scale-s resolution indicates of the the elevationNASA Shuttle in meters Radar above Topographic sea level (mMission a.s.l.) as(SRTM recorded) 90 m in Digital the raster Elevation layers ofDatabase 30-s resolution v4.1 deposited of the NASAin DIVA Shuttle-GIS ( Radarhttps://www.diva Topographic-gis.org/, Mission (SRTM)accessed 90 on m 15 Digital July 2021 Elevation). Database v4.1 deposited in DIVA-GIS (https://www.diva-gis.org/, accessed on 15 July 2021). Martínez-Domínguez et al. [7] (2016) demonstrated that populations from the Los TuxtlasMart regionínez-Dom of Veracruz,ínguez et historically al. [7] (2016) recognized demonstrated as Ceratozamia that populations robusta, from were the signifi- Los Tuxtlascantly regiondifferentiated of Veracruz, from historically other populations recognized of asC. Ceratozamiarobusta. The robusta authors, were used significantly qualitative differentiatedmorphological from traits other and populationsmolecular evidence of C. robusta to support. The authors the erection used qualitativeof a new species morpho- that logicalthey named traits C. and subroseophylla molecular evidence Mart.-Domínguez to support & the Nic. erection-Mor. In of a similar a new speciesway, populations that they namedfrom GuerreroC. subroseophylla (MexicoMart.-Dom) reportedlyínguez closely & Nic.-Mor.related to InC. arobusta similar were way, assigned populations to a from new Guerrerotaxon, C. (Mexico)leptoceras reportedlyMart.-Domínguez, closely related Nic-Mor., to C. D.W. robusta Stev.were & Lorea assigned-Hern. to a[9] new. Close taxon, in- C.spection leptoceras of Mart.-Dommorphologicalínguez, variation Nic-Mor., among D.W. populatio Stev. & Lorea-Hern.ns in Chiapas [9]. ( CloseMexico inspection) and Belize of morphologicalrevealed that the variation populations among from populations
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